Skip to main content
Log in

Neurotransmitters in subcortical somatosensory pathways

  • Review Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Investigations during recent years indicate that many different neuroactive substances are involved in the transmission and modulation of somesthetic information in the central nervous system. This review surveys recent developments within the field of somatosensory neurotransmission, emphasizing immunocytochemical findings. Increasing evidence indicates a widespread role for glutamate as a fast-acting excitatory neurotransmitter at different levels in somatosensory pathways. Several studies have substantiated a role for glutamate as a neurotransmitter in primary afferent neurons and in corticofugal projections, and also indicate a neurotransmitter role for glutamate in ascending somatosensory pathways. Other substances likely to be involved in somatosensory neurotransmission include the neuropeptides. Many different peptides have been detected in primary afferent neurons with unmyelinated or thinly myelinated axons, and are thus likely to be directly involved in primary afferent neurotransmission. Some neurons giving rise to ascending somatosensory pathways, primarily those with cell bodies in the dorsal horn, are also immunoreactive for peptides. Recent investigations have shown that the expression of neuropeptides, both in primary afferent and ascending tract neurons, may change as a result of various kinds of peripheral manipulation. The occurence of neurotransmitters in intrinsic neurons and neurons providing modulating inputs to somatosensory relay nuclei (the dorsal horn, the lateral cervical nucleus, the dorsal column nuclei and the ventrobasal thalamus) is also reviewed. Neurotransmitters and modulators in such neurons include acetylcholine, monoamines, GABA, glycine, glutamate, and various neuropeptides.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Airaksinen MS, Panula P (1988) The histaminergic system in the guinea-pig central nervous system: an immunocytochemical mapping study using an antiserum against histamine. J Comp Neurol 273:163–186

    Google Scholar 

  • Airaksinen MS, Flügge G, Fuchs E, Panula P (1989) Histaminergic system in the tree shrew brain. J Comp Neurol 286:289–310

    Google Scholar 

  • Alvarez FJ, Kavookjian AM, Light AR (1992) Synaptic interactions between GABA-immunoreactive profiles and the terminals of functionally defined myelinated nociceptors in the monkey and cat spinal cord. J Neurosci 12:2901–2917

    Google Scholar 

  • Alvarez FJ, Kavookjian AM, Light AR (1993) Ultrastructural morphology, synaptic relationships, and CGRP immunoreactivity of physiologically identified C-fiber terminals in the monkey spinal cord. J Comp Neurol 329:472–490

    Google Scholar 

  • Antal M, Polgar E, Chalmers J, Minson JB, Llewellyn-Smith I, Heizmann CW, Somogyi P (1991) Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. J Comp Neurol 314:114–124

    Google Scholar 

  • Apkarian AV, Hodge CJ (1989 a) Primate spinothalamic pathways. I. A quantitative study of the cells of origin of the spinothalamic pathway. J Comp Neurol 288:447–473

    Google Scholar 

  • Apkarian AV, Hodge CJ (1989 b) Primate spinothalamic pathways. III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways. J Comp Neurol 288:493–511

    Google Scholar 

  • Aronin N, DiFiglia M, Liotta AS, Martin JB (1981) Ultrastructural localization and biochemical features of immunoreactive leuenkephalin in monkey dorsal horn. J Neurosci 1:561–577

    Google Scholar 

  • Banna NR, Jabbur SJ (1989) Neurochemical transmission in the dorsal column nuclei. Somatosens Motor Res 6:237–251

    Google Scholar 

  • Barbaresi P, Rustioni A, Cuénod M (1985) Retrograde labeling of dorsal root ganglion neurons after injection of tritiated amino acids in the spinal cord of rats and cats. Somatosens Res 3:57–74

    Google Scholar 

  • Barbaresi P, Spreafico R, Frassoni C, Rustioni A (1986) GABA-ergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats. Brain Res 282:305–326

    Google Scholar 

  • Barber RP, Vaughn JE, Slemmon JR, Salvaterra PM, Roberts E, Leeman SE (1979) The origin, distribution and synaptic relationships of substance P axons in rat spinal cord. J Comp Neurol 184:331–352

    Google Scholar 

  • Barber RP, Vaughn JE, Roberts E (1982) The cytoarchitecture of GABAergic neurons in rat spinal cord. Brain Res 238:305–328

    Google Scholar 

  • Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1984) The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229:329–346

    Google Scholar 

  • Basbaum AI, Glazer EJ (1983) Immunoreactive vasoactive intestinal polypeptide is concentrated in sacral spinal cord: a possible marker for pelvic visceral afferent fibers. Somatosens Res 1:69–82

    Google Scholar 

  • Battaglia G, Rustioni A (1992) Substance P innervation of the rat and cat thalamus. II. Cells of origin in the spinal cord. J Comp Neurol 315:473–486

    Google Scholar 

  • Battaglia G, Spreafico R, Rustioni A (1992) Substance P innervation of the rat and cat thalamus. I. Distribution and relation to ascending spinal pathways. J Comp Neurol 315:457–472

    Google Scholar 

  • Berkley KJ (1980) Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatosensory inputs to lateral diencephalon. J Comp Neurol 193:283–317

    Google Scholar 

  • Berkley KJ, Blomqvist A, Pelt A, Flink R (1980) Differences in the collateralization of neuronal projections from the dorsal column nuclei and lateral cervical nucleus to the thalamus and tectum in the cat: an anatomical study using two different double-labeling techniques. Brain Res 202:273–290

    Google Scholar 

  • Berkley KJ, Budell RJ, Blomqvist A, Bull M (1986) Output systems of the dorsal column nuclei in the cat. Brain Res Rev 11:199–225

    Google Scholar 

  • Biella G, Panara C, Pecile A, Sotgiu ML (1991) Facilitory role of calcitonin gene-related peptide (CGRP) on excitation induced by substance P (SP) on noxious stimuli in rat spinal dorsal horn neurons. An iontophoretic study in vivo. Brain Res 559:352–356

    Google Scholar 

  • Björklund A, Skagerberg G (1979) Evidence for a major spinal cord projection from the diencephalic A11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing. Brain Res 177:170–175

    Google Scholar 

  • Blackstad TW, Karagülle T, Ottersen OP (1990) Morforel, a computer program for two-dimensional analysis of micrographs of biological specimens, with emphasis on immunogold preparations. Comput Biol Med 20:15–34

    Google Scholar 

  • Blessing WW (1990) Distribution of glutamate decarboxylase-containing neurons in rabbit medulla oblongata with attention to intramedullary and spinal projections. Neuroscience 37:171–185

    Google Scholar 

  • Blomqvist A, Broman J (1993) Serotoninergic innervation of the dorsal column nuclei and its relation to cytoarchitectonic subdivisions: an immunohistochemical study in cats and monkeys (Aotus trivirgatus). J Comp Neurol 327:584–596

    Google Scholar 

  • Blomqvist A, Flink R, Bowsher D, Griph S, Westman J (1978) Tectal and thalamic projections of dorsal column and lateral cervical nuclei: a quantitative study in the cat. Brain Res 141:335–341

    Google Scholar 

  • Blomqvist A, Flink R, Westman J, Wiberg M (1985 a) Synaptic terminals in the ventroposterolateral nucleus of the thalamus from neurons in the dorsal column and lateral cervical nulcei: an electron microscopic study in the cat. J Neurocytol 14:869–886

    Google Scholar 

  • Blomqvist A, Westman J, Köhler C, Wu J-Y (1985 b) Immunocyto-chemical localization of glutamic acid decarboxylase and substance P in the lateral cervical nucleus: a light and electron microscopic study in the cat. Neurosci Lett 56:229–233

    Google Scholar 

  • Blomqvist A, Ericson A-C, Broman J, Craig AD (1992 a) Electron microscopic identification of lamina I axon terminations in the nucleus submedius of the cat thalamus. Brain Res 585:425–430

    Google Scholar 

  • Blomqvist A, Ericson A-C, Broman J, Craig AD (1992 b) Spinothalamic tract terminals in the cat's nucleus submedius are presynaptic to GABA-immunoreactive local circuit neurons. Soc Neurosci Abstr 18:832

    Google Scholar 

  • Blomqvist A, Hermanson O, Ericson H, Larhammar D (1994) Activation of a bulbospinal opioidergic projection by pain stimuli in the awake rat. Neuroreport (in press)

  • Boivie J (1970) The termination of the cervicothalamic tract in the cat. An experimental study with silver impregnation methods. Brain Res 19:333–360

    Google Scholar 

  • Boivie J (1971) The termination of the spinothalamic tract in the cat. An experimental study with silver impregnation methods. Exp Brain Res 12:331–353

    Google Scholar 

  • Boivie J (1979) An anatomical reinvestigation of the termination of the spinothalamic tract in the monkey. J Comp Neurol 186:343–370

    Google Scholar 

  • Boivie J (1980) Thalamic projections from lateral cervical nucleus in monkey. A degeneration study. Brain Res 198:13–26

    Google Scholar 

  • Boivie J (1983) Anatomic and physiologic features of the spino-cervico-thalamic pathway. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory integration in the thalamus. Eisevier, Amsterdam, pp 63–106

    Google Scholar 

  • Bowker RM (1986) Intrinsic 5HT-immunoreactive neurons in the spinal cord of the fetal non-human primate. Dev Brain Res 28:137–143

    Google Scholar 

  • Bowker RM, Steinbusch HWM, Coulter JD (1981) Serotonergic and peptidergic projections to the spinal cord demonstrated by a combined retrograde HRP histochemical and immunocytochemical staining method. Brain Res 211:412–417

    Google Scholar 

  • Bresnahan JC, Ho RH, Beattie MS (1984) A comparison of the ultrastructure of substance P and enkephalin-immunoreactive elements in the nucleus of the dorsal lateral funioulus and laminae I and II of the rat spinal cord. J Comp Neurol 229:497–511

    Google Scholar 

  • Brodin L, Ohta Y, Hökfelt T, Grillner S (1989) Further evidence for excitatory amino acid transmission in lamprey reticulospinal neurons: selective retrograde labeling with (3H)D-aspartate. J Comp Neurol 281:225–233

    Google Scholar 

  • Broman J, Blomqvist A (1989 a) GABA-immunoreactive neurons and terminals in the lateral cervical nucleus of the cynomolgus monkey. J Comp Neurol 283:415–424

    Google Scholar 

  • Broman J, Blomqvist A (1989 b) Substance P-like immunoreactivity in the lateral cervical nucleus of the owl monkey (Aotus trivirgatus): a comparison with the cat and rat. J Comp Neurol 289:111–117

    Google Scholar 

  • Broman J, Blomqvist A (1990) Serotonergic innervation of the lateral cervical nucleus: an immunohistochemical study in cats and monkeys (Aotus trivirgatus). Synapse 6:55–62

    Google Scholar 

  • Broman J, Ottersen OP (1992) Cervicothalamic tract terminals are enriched in glutamate-like immunoreactivity: an electron microscopic double-labeling study in the cat. J Neurosci 12:204–221

    Google Scholar 

  • Craig AD Jr, Sailer S, Kniffki K-D (1987) Organization of anterogradely labeled spinocervical tract terminations in the lateral cervical nucleus of the cat. J Comp Neurol 263:214–222

    Google Scholar 

  • Cropper EC, Eisenman JS, Azmitia EC (1984) An immunocyto-chemical study of the serotonergic innervation of the thalamus of the rat. J Comp Neurol 224:38–50

    Google Scholar 

  • Cruz L, Basbaum AI (1985) Multiple opioid peptides and the modulation of pain: immunohistochemical analysis of dynorphin and enkephalin in the trigeminal nucleus caudalis and spinal cord of the cat. J Comp Neurol 240:331–348

    Google Scholar 

  • Cuénod M, Audinat B, Do KQ, Gähwiler BH, Grandes P, Herrling P, Knöpfel T, Perschak H, Streit P, Vollenweider F, Wieser HG (1990 a) Homocysteic acid as transmitter candidate in the mammalian brain and excitatory amino acids in epilepsy. Adv Exp Med Biol 268:57–63

    Google Scholar 

  • Cuénod M, Do KQ, Grandes P, Morino P, Streit P (1990 b) Localization and release of homocysteic acid, an excitatory sulphur-containing amino acid. J Histochem Cytochem 38:1713–1715

    Google Scholar 

  • Curtis DR, Johnston GAR (1974) Amino acid transmitters in the mammalian central nervous system. Ergeb Physiol 69:94–188

    Google Scholar 

  • Curtis DR, Watkins JC (1960) The excitation and depression of spinal neurones by structurally related amino acids. J Neurochem 6:117–141

    Google Scholar 

  • Curtis DR, Duggan AW, Felix D, Johnston GAR, Tebecis AK, Watkins JC (1972) Excitation of mammalian central neurones by acidic amino acids. Brain Res 41:283–301

    Google Scholar 

  • Dalsgaard CJ (1988) The sensory system. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy, vol 6. Elsevier, Amsterdam, pp 599–636

    Google Scholar 

  • Dalsgaard CJ, Haegerstrand A, Theodorsson-Norheim E, Brodin E, Hökfelt T (1985) Neurokinin A-like immunoreactivity in rat primary sensory neurons; coexistence with substance P. Histochemistry 83:37–39

    Google Scholar 

  • Dalsgaard CJ, Jernbeck J, Stains W, Kjartansson J, Haegerstrand A, Hökfelt T, Brodln E, Cuello AC, Brown JC (1989) Calcitonin gene-related peptide-like immunoreactivity in nerve fibers in the human skin. Relation to fibers containing substance P-, somatostatin- and vasoactive intestinal polypeptide-like immunoreactivity. Histochemistry 91:35–38

    Google Scholar 

  • Davies J, Watkins JC (1973 a) Antagonism of synaptic and amino acid induced excitation in the cuneate nucleus of the cat by HA-966. Neuropharmacology 12:637–640

    Google Scholar 

  • Davies J, Watkins JC (1973 b) Microelectrophoretic studies on the depressant action of HA-966 on chemically and synaptically excited neurones in the cat cerebral cortex and cuneate nucleus. Brain Res 59:311–322

    Google Scholar 

  • Davies SN, Lodge D (1987) Evidence for involvement of N-methylaspartate receptors in “wind-up” of class 2 neurones in the dorsal horn of the rat. Brain Res 424:402–406

    Google Scholar 

  • De Biasi S, Rustioni A (1988) Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc Natl Acad Sci USA 85:7820–7824

    Google Scholar 

  • De Biasi S, Rustioni A (1990) Ultrastructural immunocytochemical localization of excitatory amino acids in the somatosensory system. J Histochem Cytochem 38:1745–1754

    Google Scholar 

  • De Biasi S, Frassoni C, Spreafico R (1986) GABA immunoreactivity in the thalamic reticular nucleus of the rat. A light and electron microscopical study. Brain Res 399:143–147

    Google Scholar 

  • De Biasi S, Frassoni C, Spreafico R (1988) The intrinsic organization of the ventroposterolateral nucleus and related reticular thalamic nucleus of the rat: a double-labeling ultrastructural investigation with γ-aminobutyric acid immunogold staining and lectin-conjugated horseradish peroxidase. Somatosens Res 5:187–203

    Google Scholar 

  • De Biasi S, Vitellaro-Zuccarello L, Bernardi P, Rustioni A (1991) Post-synaptic dorsal column terminals in the cuneate nucleus of the rat: morphology and putative transmitter. Soc Neurosci Abstr 17:289

    Google Scholar 

  • De Biasi S, Vitellaro-Zuccarello L, Bernardi P (1992) Ultrastructural characterization of synaptic terminals in the rat cuneate nucleus. Soc Neurosci Abstr 18:1017

    Google Scholar 

  • DeGroat WC, Kawatani M, Hisamitsu T, Lowe I, Morgan C, Rappolo J, Both AM, Nadelhaft I (1983) The role of neuropeptides in the sacral autonomic pathways of the cat. J Auton Nerv Syst 7:339–350

    Google Scholar 

  • De Koninck Y, Henry JL (1989) Bombesin, neuromedin B and neuromedin C selectively depress superficial dorsal horn neurones in the cat spinal cord. Brain Res 498:105–117

    Google Scholar 

  • De Koninck Y, Henry JL (1992) Peripheral vibration causes an adenosine-mediated postsynaptic inhibitory potential in dorsal horn neurons of the cat spinal cord. Neuroscience 50:435–443

    Google Scholar 

  • De Koninck Y, Ribeiro-da-Silva A, Henry JL, Cuello AC (1992) Spinal neurons exhibiting a specific nociceptive response receive abundant substance P-containing synaptic contacts. Proc Natl Acad Sci USA 89:5073–5077

    Google Scholar 

  • De Lanerolle NC, LaMotte CC (1982) Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. I. Substance P immunoreactivity. Brain Res 274:31–49

    Google Scholar 

  • De Leon M, Covenas R, Narvaez JA, Tramu G, Aguirre JA, Gonzalez-Baron S (1991) Somatostatin-28 (1–12)-like immunoreactivity in the cat diencephalon. Neuropeptides 19:107–117

    Google Scholar 

  • Deschénes M, Hu B (1990) Electrophysiology and pharmacology of the corticothalamic input to lateral thalamic nuclei: an intracellular study in the cat. Eur J Neurosci 2:140–152

    Google Scholar 

  • Dickenson AH, Sullivan A (1990) Differential effects of excitatory amino acid antagonists on dorsal horn nociceptive neurones in the rat. Brain Res 506:31–39

    Google Scholar 

  • DiFiglia M, Aronin N, Leeman SE (1982) Light microscopic and ultrastructural localization of immunoreactive substance P in the dorsal horn of the monkey spinal cord. Neuroscience 7:1127–1139

    Google Scholar 

  • Donaldson LF, Harmar AJ, McQueen DS, Seckl JR000 (1992) Increased expression of preprotachykinin, calcitonin gene-related peptide, but not vasoactive intestinal peptide messenger RNA in dorsal root ganglia during the development of adjuvant monoarthritis in the rat. Mol Brain Res 16:143–149

    Google Scholar 

  • Dostrovsky JO (1984) Brainstem influences on transmission of somatosensory information in the spinocervicothalamic pathway. Brain Res 292:229–238

    Google Scholar 

  • Dougherty PM, Willis WD (1991) Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined micro-iontophoretic application of N-methyl-D-aspartic acid and substance P. Pain 47:85–93

    Google Scholar 

  • Dougherty PM, Palecek J, Paleckova V, Sorkin LS, Willis WD (1992) The role of NMDA and non-NMDA excitatory amino acid receptors in the excitation of primate spinothalamic tract neurons by mechanical, chemical, thermal, and electrical stimuli. J Neurosci 12:3025–3041

    Google Scholar 

  • Downie JW, Ferrington DG, Sorkin LS, Willis WD (1988) The primate spinocervicothalamic pathway: responses of cells of the lateral cervical nucleus and spinocervical tract to innocuous and noxious stimuli. J Neurophysiol 59:861–885

    Google Scholar 

  • Doyle CA, Maxwell DJ (1991) Ultrastructural analysis of noradrenergic nerve terminals in the cat lumbosacral spinal dorsal horn: a dopamine-β-hydroxylase immunocytochemical study. Brain Res 563:329–333

    Google Scholar 

  • Dubner R, Ruda MA (1992) Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15:96–103

    Google Scholar 

  • Duggan AW, Johnston GAR (1970) Glutamate and related amino acids in cat spinal roots, dorsal root ganglia and peripheral nerves. J Neurochem 17:1205–1208

    Google Scholar 

  • Duggan AW, Hall JG, Headley PM (1976) Morphine, enkephalin and the substantia gelatinosa. Nature 264:456–458

    Google Scholar 

  • Duggan AW, Hall JG, Headley PM (1977) Enkephalins and dorsal horn neurones of the cat: effects on responses to noxious and innocuous skin stimuli. Br J Pharmacol 61:399–408

    Google Scholar 

  • Eaton SA, Salt TE (1991) Membrane and action potential responses evoked by excitatory amino acids acting at N-methyl-D-aspartate receptors and non-N-methyl-D-aspartate receptors in the rat thalamus in vivo. Neuroscience 44:277–286

    Google Scholar 

  • Eaton SA, Birse EF, Wharton B, Sunter DC, Udvarhelyi PM, Watkins JC, Salt TE (1993) Mediation of thalamic sensory responses in vivo by ACPD-activated excitatory amino acid receptors. Eur J Neurosci 5:186–189

    Google Scholar 

  • Edwards DL, Poletti CE, Foote WE (1987) Evidence for leucineenkephalin immunoreactive neurons in the medulla which project to the spinal cord in squirrel monkey. Brain Res 437:197–203

    Google Scholar 

  • Edwards FA, Gibb AJ, Colquhoun D (1992) ATP receptor-mediated synaptic currents in the central nervous system. Nature 359:144–146

    Google Scholar 

  • Ericson A-C, Blomqvist A, Craig AD, Ottersen OP, Broman J (1992) Enrichment of glutamate-like immunoreactivity in spinothalamic tract terminals in the nucleus submedius of cat. Soc Neurosci Abstr 18:832

    Google Scholar 

  • Ericson A-C, Broman J, Blomqvist A (1993) Glutamate-like immunoreactivity in primate spinothalamic tract terminals. Soc Neurosci Abstr 19:1571

    Google Scholar 

  • Ericson H, Watanabe T, Köhler C (1987) Morphological analysis of the tuberomammillary nucleus in the rat brain: delineation of subgroups with antibody against L-histidine decarboxylase as a marker. J Comp Neurol 263:1–24

    Google Scholar 

  • Erulkar SD (1989) Chemically mediated synaptic transmission: an overview. In: Siegel GJ, Agranoff BW, Albers RW, Molinoff PB (eds) Basic neurochemistry: molecular, cellular, and medical aspects, 4th edn. Raven Press, New York, pp 151–182

    Google Scholar 

  • Evans RJ, Derkach V, Surprenant A (1992) ATP mediates fast synaptic transmission in mammalian neurons. Nature 357:503–505

    Google Scholar 

  • Fabri M, Conti F (1990) Calcitonin gene-related peptide-positive neurons and fibers in the cat dorsal column nuclei. Neuroscience 35:167–174

    Google Scholar 

  • Fitzpatrick D, Diamond IT, Raczkowski D (1989) Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J Comp Neurol 288:647–675

    Google Scholar 

  • Fleetwood-Walker SM, Mitchell R, Hope PJ, Molony V, Iggo A (1985) An apha2 receptor mediates the selective inhibition by noradrenaline of nociceptive responses of identified dorsal horn neurones. Brain Res 334:243–254

    Google Scholar 

  • Fleetwood-Walker SM, Hope PJ, Mitchell R (1988 a) Antinociceptive actions of descending dopaminergic tracts on cat and rat dorsal horn somatosensory neurones. J Physiol (Lond) 399:335–348

    Google Scholar 

  • Fleetwood-Walker SM, Hope PJ, Mitchell R, El-Yassir N, Molony V (1988 b) The influence of opioid receptor subtypes on the processing of nociceptive inputs in the dorsal horn of the cat. Brain Res 451:213–226

    Google Scholar 

  • Flink R, Westman J (1986) Different neuron populations in the feline lateral cervical nucleus: a light and electron microscopic study with the retrograde axonal transport technique. J Comp Neurol 250:265–281

    Google Scholar 

  • Flink R, Wiberg M, Blomqvist A (1983) The termination in the mesencephalon of fibres from the lateral cervical nucleus. An anatomical study in the cat. Brain Res 259:11–20

    Google Scholar 

  • Florence SL, Wall JT, Kaas JH (1988) Somatotopic organization of inputs from the hand to the spinal gray and cuneate nucleus of monkeys with observations on the cuneate nucleus in humans. J Comp Neurol 286:48–70

    Google Scholar 

  • Franco-Cereceda A, Henke H, Lundberg JM, Petermann JB, Hökfelt T, Fischer JA (1987) Calcitonin gene-related peptide (CGRP) in capsaicin-sensitive substance P-immunoreactive neurons in animals and man: distribution and release by capsaicin. Peptides 8:399–410

    Google Scholar 

  • Fritschy J-M, Grzanna R (1990) Demonstration of two separate descending noradrenergic pathways to the rat spinal cord: evidence for an intragriseal trajectory of locus coeruleus axons in the superficial layers of the dorsal horn. J Comp Neurol 291:553–582

    Google Scholar 

  • Fyffe REW, Perl ER (1984) Is ATP a central synaptic mediator for certain primary afferent fibres from mammalian skin? Proc Natl Acad Sci USA 81:6890–6893

    Google Scholar 

  • Galindo A, Krnjevic K, Schwartz S (1967) Microiontophoretic studies on neurones in the cuneate nucleus. J Physiol (Lond) 192:359–377

    Google Scholar 

  • Gerber G, Randic M (1989) Excitatory amino acid-mediated components of synaptically evoked input from dorsal roots to deep dorsal horn neurons in the rat spinal cord slice. Neurosci Lett 106:211–219

    Google Scholar 

  • Gerber G, Cerne R, Randic M (1991) Participation of excitatory amino acid receptors in the slow excitatory synaptic transmission in rat spinal dorsal horn. Brain Res 561:236–251

    Google Scholar 

  • Gibbins IL, Furness JB, Costa M (1987) Pathway-specific patterns of the coexistence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 248:417–437

    Google Scholar 

  • Gibson SJ, Polak JM, Giaid A, Hamid QA, Kar S, Jones PM, Denny P, Legon S, Amara SG, Craig RK, Bloom SR, Penketh RJA, Rodek C, Ibrahim NBN, Dawson A (1988) Calcitonin gene-related peptide messenger RNA is expressed in sensory neurons of the dorsal root ganglia and also in spinal motoneurons in man and rat. Neurosci Lett 91:283–288

    Google Scholar 

  • Giesler GJ Jr, Elde RP (1985) Immunocytochemical studies of the peptidergic content of fibers and terminals within the lateral spinal and lateral cervical nuclei. J Neurosci 5:1833–1841

    Google Scholar 

  • Giesler GJ Jr, Björkeland M, Xu Q, Grant G (1988) Organization of the spinocervicothalamic pathway in the rat. J Comp Neurol 268:223–233

    Google Scholar 

  • Giuffrida R, Rustioni A (1992) Dorsal root ganglion neurons projecting to the dorsal column nuclei of rats. J Comp Neurol 316:206–220

    Google Scholar 

  • Giuffrida R, De Biasi S, Bellomo M, Rustioni A (1991) Glutamate immunostaining in the dorsal column system of rats. Soc Neurosci Abstr 17:1004

    Google Scholar 

  • Glazer EJ, Basbaum AI (1981) Immunohistochemical localization of leucine-enkephalin in the spinal cord of the cat: enkephalin-containing marginal neurons and pain modulation. J Comp Neurol 196:377–389

    Google Scholar 

  • Goldfinger MD, Hensley S, Schmalholz D (1985) Recovery and detection of amino acids released within the cat cuneate nucleus. Soc Neurosci Abstr 11:561

    Google Scholar 

  • Gordon G, Jukes MGM (1963) An investigation of cells in the lateral cervical nucleus of the cat which respond to stimulation of the skin. J Physiol (Lond) 169:28–29

    Google Scholar 

  • Graham LT, Shank RP, Werman R, Aprison MH (1967) Distribution of some transmitter suspects in cat spinal cord: glutamic acid, aspartic acid, gamma-aminobutyric acid, glycine and glutamine. J Neurochem 14:465–472

    Google Scholar 

  • Grandes P, Do KQ, Morino P, Cuénod M, Streit P (1991) Homocysteate, an excitatory transmitter candidate localized in glia. Eur J Neurosci 3:1370–1373

    Google Scholar 

  • Griffiths R (1990) Cysteine sulphinate (CSA) as an excitatory amino acid transmitter candidate in the mammalian central nervous system. Prog Neurobiol 35:313–323

    Google Scholar 

  • Haldeman S, Huffman RD, Marshall KC, McLennan H (1972) The antagonism of the glutamate-induced and synaptic excitation of thalamic neurones. Brain Res 39:419–425

    Google Scholar 

  • Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262:105–124

    Google Scholar 

  • Hallanger AE, Price SD, Lee HJ, Steininger TL, Wainer BH (1990) Ultrastructure of cholinergic synaptic terminals in the thalamic anteroventral, ventroposterior, and dorsal lateral geniculate nuclei of the rat. J Comp Neurol 299:482–492

    Google Scholar 

  • Hamori J, Takacs J, Verley R, Petrusz P, Farkas-Bargeton E (1990) Plasticity of GABA- and glutamate-containing terminals in the mouse thalamic ventrobasal complex deprived of vibrissal afferents: an immunogold-electron microscopic study. J Comp Neurol 302:739–748

    Google Scholar 

  • Harrison PJ, Jankowska E (1984) An intracellular study of descending and non-cutaneous afferent input to spinocervical tract neurones in the cat. J Physiol (Lond) 356:245–261

    Google Scholar 

  • Hayes ES, Carlton SM (1992) Primary afferent interactions: analysis of calcitonin gene-related peptide-immunoreactive terminals in contact with unlabeled and GABA-immunoreactive profiles in the monkey dorsal horn. Neuroscience 47:873–896

    Google Scholar 

  • Heckers S, Guela C, Mesulam M-M (1992) Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J Comp Neurol 325:68–82

    Google Scholar 

  • Heino R, Westman J (1991) Quantitative analysis of the feline dorsal column nuclei and their GABAergic and non-GABAergic neurons. Anat Embryol 184:181–193

    Google Scholar 

  • Henderson Z, Salt TE (1988) The effects of N-acetylaspartylglutamate and distribution of N-acetylaspartylglutamate-like immunoreactivity in the rat somatosensory thalamus. Neuroscience 25:899–906

    Google Scholar 

  • Henry JL (1976) Effects of substance P on functionally identified units in cat spinal cord. Brain Res 114:439–451

    Google Scholar 

  • Hicks TP, Kaneko T, Metherate R, Oka J-I, Stark CA (1991) Amino acids as transmitters of synaptic excitation in neocortical sensory processes. Can J Physiol Pharmacol 69:1099–1114

    Google Scholar 

  • Hirai T, Jones EG (1989) Distribution of tachykinin- and enkephalin-immunoreactive fibers in the human thalamus. Brain Res Rev 14:35–52

    Google Scholar 

  • Hirata H, Pubols BH Jr (1989) Spinocervical tract neurons responsive to light mechanical stimulation of the raccoon forepaw. J Neurophysiol 61:138–148

    Google Scholar 

  • Hökfelt T, Kellerth JO, Nilsson G, Pernow B (1975a) Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurons. Brain Res 100:235–252

    Google Scholar 

  • Hökfelt T, Elde R, Johansson O, Luft R, Arimura A (1975b) Immunohistochemical evidence for the presence of somatostatin, a powerful inhibitory peptide, in some primary sensory neurons. Neurosci Lett 1:231–235

    Google Scholar 

  • Hökfelt T, Elde K, Johansson O, Terenius L, Stein L (1977) The distribution of enkephalin immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 5:25–32

    Google Scholar 

  • Hökfelt T, Phillipson O, Goldstein M (1979) Evidence for a dopaminergic pathway in the rat descending from the All cell group to the spinal cord. Acta Physiol Scand 107:393–395

    Google Scholar 

  • Hökfelt T, Herrera-Marschitz M, Seroogy K, Ju G, Staines WA, Holets V, Schalinng M, Ungerstedt U, Post C, Rehfeld JF, Frey P, Fischer J, Dockray G, Hamaoka T, Walsh JH, Goldstein M (1988) Immunohistochemical studies on cholecystokinin (CCK)-immunoreactive neurons in the rat using sequence specific antisera and with special reference to the caudate nucleus and primary sensory neurons. J Chem Neuroanat 1:11–52

    Google Scholar 

  • Hökfelt T, Verge VMK, Wiesenfeld-Hallin Z, Eriksson M (1991) Upregulation of vasoactive intestinal polypeptide in substance P expressing primary sensory neurons after injury. Soc Neurosci Abstr 17:439

    Google Scholar 

  • Hoffert MJ, Miletic V, Ruda MA, Dubner R (1983) Immunocytochemical identification of serotonin axonal contacts on characterized neurons in laminae I and II of the cat dorsal horn. Brain Res 267:361–364

    Google Scholar 

  • Holstege JC (1991) Ultrastructural evidence for GABAergic brain stem projections to spinal motoneurons in the rat. J Neurosci 11:159–167

    Google Scholar 

  • Holstege JC, Bongers CMH (1991) A glycinergic projection from the ventromedial lower brainstem to spinal motoneurons. An ultrastructural double labeling study in rat. Brain Res 566:308–315

    Google Scholar 

  • Hori Y, Endo K (1992) Miniature postsynaptic currents recorded from identified rat spinal dorsal horn projection neurons in thin-slice preparations. Neurosci Lett 142:191–195

    Google Scholar 

  • Hori Y, Endo K, Takahashi T (1992) Presynaptic inhibitory action of enkephalin on excitatory transmission in superficial dorsal horn of rat spinal cord. J Physiol (Lond) 450:673–685

    Google Scholar 

  • Horrobin DF (1966) The lateral cervical nucleus of the cat; an electrophysiological study. Q J Exp Physiol 51:351–371

    Google Scholar 

  • Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the main cell type of the nucleus reticularis thalami. Brain Res 200:341–354

    Google Scholar 

  • Hunt CA, Seroogy KB, Gall CM, Jones EG (1987) Cholecystokinin innervation of rat thalamus, including fibers to ventroposterolateral nucleus from dorsal column nuclei. Brain Res 426:257–269

    Google Scholar 

  • Hunt CA, Pang DZ, Jones EG (1991) Distribution and density of GABA cells in intralaminar and adjacent nuclei of monkey thalamus. Neuroscience 43:185–196

    Google Scholar 

  • Hunt SP (1983) Cytochemistry of the spinal cord. In: Emson PC (ed) Chemical neuroanatomy. Raven Press, New York, pp 53–84

    Google Scholar 

  • Hunt SP, Kelly JS, Emson PC, Kimmel JR, Miller RJ, Wu JY (1981) An immunohistochemical study of neuronal populations containing neuropeptides or γ-aminobutyrate within the superficial layers of the rat dorsal horn. Neuroscience 6:1883–1898

    Google Scholar 

  • Huxtable RJ (1989) Taurine in the central nervous system and the mammalian actions of taurine. Prog Brain Res 32:471–533

    Google Scholar 

  • Hylden JLK, Hayashi H, Ruda MA, Dubner R (1986) Serotonin innervation of physiologically identified lamina I projection neurons. Brain Res 370:401–404

    Google Scholar 

  • Inagaki N, Yamatodani A, Ando-Yamamoto M, Tohyama M, Watanabe T, Wada H (1988) Organization of histaminergic fibers in the rat brain. J Comp Neurol 273:283–300

    Google Scholar 

  • Ishida-Yamamoto A, Senba E (1990) Cell types and axonal sizes of calcitonin gene-related peptide-containing primary sensory neurons of the rat. Brain Res Bull 24:759–764

    Google Scholar 

  • Jahr CE, Jessell TM (1983) ATP excites a subpopulation of rat dorsal horn neurones. Nature 304:730–733

    Google Scholar 

  • Jahr CE, Yoshioka K (1986) Ia afferent excitation of motoneurones in the in vitro new-born rat spinal cord is selectively antagonized by kynurenate. J Physiol (Lond) 370:515–530

    Google Scholar 

  • Jansco G, Hökfelt T, Lundberg JM, Kiraly E, Halasz N, Nilsson G, Terenius L, Rehfeld J, Steinbusch H, Verhofstad A, Elde R, Said S, Brown M (1981) Immunohistochemical studies on the effect of capsaicin on spinal and medullary peptide and monoamine neurons using antisera to substance P, gastrin/CCK, somatostatin, VIP, enkephalin, neurotensin and 5-hydroxytryptamine. J Neurocytol 19:963–980

    Google Scholar 

  • Jeftinija S, Miletic V, Randic M (1981) Cholecystokinin octapeptide excites dorsal horn neurons both in vivo and in vitro. Brain Res 213:231–236

    Google Scholar 

  • Jeftinija S, Murase K, Nedeljikov V, Randic M (1982) Vasoactive intestinal polypeptide excites mammalian dorsal horn neurons both in vivo and in vitro. Brain Res 243:158–164

    Google Scholar 

  • Jeftinija S, Urban L, Kangrga I, Ryu PD, Randic M (1987) Slow excitatory and inhibitory transmission in the rat spinal dorsal horn in vitro and depressant effect of enkephalins. Neurol Neurobiol 28:271–281

    Google Scholar 

  • Jeftinija S, Jeftinija K, Liu F, Skilling SR, Smullin DH, Larson AA (1991) Excitatory amino acids are released from primary afferent neurons in vitro. Neurosci Lett 125:191–194

    Google Scholar 

  • Jessell T, Tsunoo A, Kanazawa I, Otsuka M (1979) Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res 168:247–259

    Google Scholar 

  • Jessell TM, Yoshioka K, Jahr CE (1986) Amino acid receptor-mediated transmission at primary afferent synapses in rat spinal cord. J Exp Biol 124:239–258

    Google Scholar 

  • Jones BE, Holmes CJ, Rodriguez-Veiga E, Mainville L (1991) GABA-synthesizing neurons in the medulla: their relationship to serotonin-containing and spinally projecting neurons in the rat. J Comp Neurol 313:349–367

    Google Scholar 

  • Jones EG (1985) The thalamus. Plenum Press, New York

    Google Scholar 

  • Jones EG (1987) Immunocytochemical studies on thalamic afferent transmitters. In: Besson J-M, Guilbaud G, Peschanski M (eds) Thalamus and pain. Elsevier, Amsterdam, pp 83–109

    Google Scholar 

  • Jones EG (1991) The anatomy of sensory relay functions in the thalamus. Prog Brain Res 87:29–52

    CAS  Google Scholar 

  • Jones SL, Light AR (1990) Termination patterns of serotoninergic medullary raphespinal fibers in the rat lumbar spinal cord: and anterograde immunohistochemical study. J Comp Neurol 297:267–282

    Google Scholar 

  • Jordan LM, Kenshalo DR Jr, Martin RF, Haber LH, Willis WD (1978) Depression of primate spinothalamic tract neurons by iontophoretic application of 5-hydroxytryptamine. Pain 5:135–142

    Google Scholar 

  • Ju G, Hökfelt T, Fischer JA, Frey P, Rehfeld JF, Dockray GJ (1986) Does cholecystokinin-like immunoreactivity in rat primary sensory neurones represent calcitonin gene-related peptide? Neurosci Lett 68:305–310

    Google Scholar 

  • Ju G, Melander T, Ceccatelli S, Hökfelt T, Frey P (1987) Immuno-histochemical evidence for a spinothalamic pathway co-containing cholecystokinin- and galanin-like immunoreactivities in the rat. Neuroscience 20:439–456

    Google Scholar 

  • Kaduri AJ, Magoul R, Lescaudron L, Campistron G, Calas A (1987) Immunocytochemical approach of GABAergic innervation of the mouse spinal cord using antibodies to GABA. J Hirnforsch 28:349–355

    Google Scholar 

  • Kai-Kai MA, Susann RW, Keen P (1985) Localization of chromatographically characterized oxytocin and arginine-vasopressin to sensory neurones in the rat. Neurosci Lett 55:83–88

    Google Scholar 

  • Kai-Kai MA, Anderton BH, Keen P (1986) A quantitative analysis of the interrelationships between subpopulations of rat sensory neurons containing arginine vasopressin or oxytocin and those containing substance P, fluoride-resistant acid phosphatase or neurofilament protein. Neuroscience 18:475–486

    Google Scholar 

  • Kajander KC, Giesler GJ Jr (1987) Responses of neurons in the lateral cervical nucleus of the cat to noxious cutaneous stimulation. J Neurophysiol 57:1686–1704

    Google Scholar 

  • Kangrga I, Randic M (1990) Tachykinins and calcitonin gene-related peptide enhance release of endogenous glutamate and aspartate from the rat spinal dorsal horn slice. J Neurosci 10:2026–2038

    Google Scholar 

  • Kangrga I, Randic M (1991) Outflow of endogenous aspartate and glutamate from the rat spinal dorsal horn in vitro by activation of low- and high-threshold primary afferent fibers. Modulation by μ-opioids. Brain Res 553:347–352

    Google Scholar 

  • Kangrga I, Larew JSA, Randic M (1990) The effects of substance P and calcitonin gene-related peptide on the efflux of endogenous glutamate and aspartate from the rat spinal dorsal horn in vitro. Neurosci Lett 108:155–160

    Google Scholar 

  • Kawagoe R, Onodera K, Takeuchi A (1986) The release of endogenous glutamate from the newborn rat spinal cord induced by dorsal root stimulation and substance P. Biomed Res 7:253–259

    Google Scholar 

  • Kawatani M, Lowe IP, Nadelhaft I, Morgan C, DeGroat WC (1983) Vasoactive intestinal polypeptide in visceral afferent pathways to the sacral spinal cord of the cat. Neurosci Lett 42:311–316

    Google Scholar 

  • Kechagias S, Broman J (1993) Further evidence for glutamate as a spinocervical tract neurotransmitter: immunogold analysis of glutamate and glutamine in the cat lateral cervical nucleus. Soc Neurosci Abstr 19:328

    Google Scholar 

  • Kechagias S, Broman J (1994) Compartmentation of glutamate and glutamine in the lateral cervical nucleus: further evidence for glutamate as a spinocervical tract neurotransmitter. J Comp Neurol (in press)

  • Kelly JS, Renaud LP (1973) On the pharmacology of the glycine receptors on cuneo-thalamic relays cells in the cat. Br J Pharmacol 48:387–395

    Google Scholar 

  • Khachaturian H, Watson SJ, Lewis ME, Coy D, Goldstein A, Akil H (1982) Dynorphin immunocytochemistry in the rat central nervous system. Peptides 3:941–954

    Google Scholar 

  • Kharazia VN, Rustioni A, Weinberg RJ (1992) Glutamate and aspartate immunoreactivity in terminals of thalamocortical fibers. Soc Neurosci Abstr 18:1387

    Google Scholar 

  • Kharazia VN, Rustioni A, Weinberg RJ (1993) Immunocytochemistry of thalamocortical terminals in layers I and IV. Soc Neurosci Abstr 19:1567

    Google Scholar 

  • Kim JHK, Kim SU, Kito S (1984) Immunocytochemical demonstration of β-endorphin and β-lipotropin in cultured human spinal ganglia neurons. Brain Res 304:192–196

    Google Scholar 

  • King AE, Thompson SWN, Urban L, Woolf CJ (1988) An intracellular analysis of amino acid induced excitations of deep dorsal horn neurons in the rat spinal cord slice. Neurosci Lett 89:286–292

    Google Scholar 

  • Klein CM, Westlund KN, Coggeshall RE (1990) Percentages of dorsal root axons immunoreactive for galanin are higher than those immunoreactive for calcitonin gene-related peptide in the rat. Brain Res 519:97–101

    Google Scholar 

  • Klockgether T (1987) Excitatory amino acid receptor-mediated transmission of somatosensory evoked potentials in the rat thalamus. J Physiol (Lond) 394:445–461

    Google Scholar 

  • Knyihar-Csillik E, Csillik B, Rakic P (1982) Periterminal synaptology of dorsal root glomerular terminals in the substantia gelatinosa of the spinal cord in the Rhesus monkey. J Comp Neurol 210:376–399

    Google Scholar 

  • Kojima M, Takeuchi Y, Goto M, Sano Y (1983) Immunohistochemical study on the localization of serotonin fibers and terminals in the spinal cord of the monkey (Macaca fuscata). Cell Tissue Res 229:23–36

    Google Scholar 

  • Kojima N, Kanazawa I (1987) Possible neurotransmitters of the dorsal column afferents: effects of dorsal column transection in the cat. Neuroscience 23:263–274

    Google Scholar 

  • Kolston J, Osen KK, Hackney CM, Ottersen OP, Storm-Mathisen J (1992) An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea-pig. Anat Embryol 186:443–465

    Google Scholar 

  • Kritzer MF, Cowey A, Ottersen OP, Streit P, Somogyi P (1992) Immunoreactivity for taurine identifies subsets of glia, GABAergic and non-GABAergic neurons in the neo- and archicortex of the rat, cat and rhesus monkey: comparison with immunoreactivity for homocysteic acid. Eur J Neurosci 4:251–270

    Google Scholar 

  • Krnjevic K, Morris ME (1974) An excitatory action of substance P on cuneate neurones. Can J Physiol Pharmacol 52:736–744

    Google Scholar 

  • Kruger L, Sternini C, Brecha NC, Mantyh PW (1988) Distribution of calcitonin gene-related peptide immunoreactivity in relation to the rat central somatosensory projection. J Comp Neurol 273:149–162

    Google Scholar 

  • Kummer W, Heym C (1986) Correlation of neuronal size and peptide immunoreactivity in the guinea-pig trigeminal ganglion. Cell Tissue Res 245:657–665

    Google Scholar 

  • Kwiat GC, Basbaum AI (1992) The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens Motor Res 9:157–173

    Google Scholar 

  • LaMotte CC (1985) Ultrastructure of peptidergic and serotonergic synaptic terminals contacting spinothalamic and other lamina V neurons of the monkey cervical cord. Soc Neurosci Abstr 11:578

    Google Scholar 

  • LaMotte CC, De Lanerolle NC (1983a) Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. II. Methionine-enkephalin immunoreactivity. Brain Res 274:51–63

    Google Scholar 

  • LaMotte CC, De Lanerolle NC (1983b) Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. III. Serotonin immunoreactivity. Brain Res 274:65–77

    Google Scholar 

  • LaMotte CC, Pert CB, Snyder SH (1976) Opiate receptor binding in primate spinal cord: distribution and changes after dorsal root section. Brain Res 112:407–412

    Google Scholar 

  • LaMotte CC, Carlton SM, Honda CN, Surmeier DJ, Willis WD (1988) Innervation of identified spinothalamic tract neurons: ultrastructure of serotonergic and other synaptic profiles. Soc Neurosci Abstr 14:852

    Google Scholar 

  • Lang RE, Heil J, Ganten D, Hermann K, Rascher W, Unger T (1983) Effects of lesions in the paraventricular nucleus of the hypothalamus on vasopressin and oxytocin contents in brain stem and spinal cord of rat. Brain Res 260:326–329

    Google Scholar 

  • Lavoie B, Parent A (1991) Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J Comp Neurol 312:1–18

    Google Scholar 

  • Leah JD, Cameron AA, Kelly WL, Snow PJ (1985 a) Coexistence of peptide immunoreactivity in sensory neurons of the cat. Neuroscience 16:683–690

    Google Scholar 

  • Leah JD, Cameron AA, Snow PJ (1985 b) Neuropeptides in physiologically identified mammalian sensory neurones. Neurosci Lett 56:257–264

    Google Scholar 

  • Leah J, Menetrey D, de Pommery J (1988) Neuropeptides in long ascending spinal tract cells in the rat: evidence for parallel processing of ascending information. Neuroscience 24:195–207

    Google Scholar 

  • Lee IS, Renno WM, Beitz AJ (1992) A quantitative light and electron microscopic analysis of taurine-like immunoreactivity in the dorsal horn of the rat spinal cord. J Comp Neurol 321:65–82

    Google Scholar 

  • Le Greve P, Nyberg F, Terenius L, Hökfelt T (1985) Calcitonin gene-related peptide is a potent inhibitor of substance P degradation. Eur J Pharmacol 115:309–311

    Google Scholar 

  • Lekan H, Hayes ES, Westlund KN, Zhang D, Willis WD, Carlton SM (1990) Analysis of GABAergic and glycinergic input to spinothalamic tract cells in primate dorsal horn. Soc Neurosci Abstr 16:704

    Google Scholar 

  • Lembeck F, Donnerer J, Colpaert FC (1981) Increase in substance P in primary afferent nerves during chronic pain. Neuropeptides 1:175–180

    Google Scholar 

  • Levey AI, Hallanger AE, Wainer BH (1987) Choline acetyltransferase immunoreactivity in the rat thalamus. J Comp Neurol 257:317–332

    Google Scholar 

  • Li J, Perl ER (1991) L-glutamate and adenosine-5′-triphosphate actions on substantia gelatinosa neurons. Soc Neurosci Abstr 17:1006

    Google Scholar 

  • Light AR, Durcovic RG (1984) Features of laminar and somatotopic organization of lumbar spinal cord units receiving cutaneous input from hindlimb receptive fields. J Neurophysiol 52:449–458

    Google Scholar 

  • Light AR, Kavookjian AM, Petrusz P (1983) The ultrastructure and synaptic connections of serotonin-immunoreactive terminals in spinal laminae I and II. Somatosens Res 1:33–50

    CAS  PubMed  Google Scholar 

  • Liu X-B, Jones EG (1991) The fine structure of serotonin and tyrosine hydroxylase immunoreactive terminals in the ventral posterior thalamic nucleus of cat and monkey. Exp Brain Res 85:507–518

    Google Scholar 

  • Lundberg JM, Hökfelt T, Nilsson G, Terenius L, Rehfelt J, Elde R, Said S (1978) Peptide neurons in the vagus, splanchnic and sciatic nerves. Acta Physiol Scand 104:499–501

    Google Scholar 

  • Lynn B, Hunt S (1984) Afferent C-fibres: physiological and biochemical correlations. Trends Neurosci 7:186–188

    Google Scholar 

  • Ma W, Ohara PT (1987) Synaptic glomeruli in the nucleus submedius of the rat thalamus. Brain Res 415:331–336

    Google Scholar 

  • Ma W, Peschanski M, Ohara PT (1988) Fine structure of the dorsal part of the nucleus submedius of the rat thalamus: an anatomical study with reference to possible pain pathways. Neuroscience 26:147–159

    Google Scholar 

  • Madarasz M, Somogyi G, Somogyi J, Hamori J (1985) Numerical estimation of γ-aminobutyric acid (GABA)-containing neurons in three thalamic nuclei of the cat: direct GABA immunocytochemistry. Neurosci Lett 61:73–78

    Google Scholar 

  • Magoul R, Onteniente B, Geffard M, Calas A (1987) Anatomical distribution and ultrastructural organization of the GABAergic system in the rat spinal cord. An immunocytochemical study using anti-GABA antibodies. Neuroscience 20:1001–1009

    Google Scholar 

  • Marlier L, Sandillon F, Poulat P, Rajaofetra N, Geffard M, Privat A (1991) Serotonergic innervation of the dorsal horn of rat spinal cord: light and electron microscopic immunocytochemical study. J Neurocytol 20:310–322

    Google Scholar 

  • Martin GF, DeLorenzo G, Ho RH, Humbertson AO Jr, Waltzer R (1986) Serotonergic innervation of the forebrain in the North American opossum. Brain Behav Evol 26:196–228

    Google Scholar 

  • Massari VJ, Tizabi Y, Park CH, Moddy TW, Heike CJ, O'Donohue TL (1983) Distribution and origin of bombesin, substance P and somatostatin in cat spinal cord. Peptides 4:673–681

    Google Scholar 

  • Maxwell DJ, Fyffe REW, Brown AG (1982) Fine structure of spinocervical tract neurons and the boutons in contact with them. Brain Res 233:394–399

    Google Scholar 

  • Maxwell DJ, Fyffe REW, Brown AG (1984) Fine structure of normal and degenerating primary afferent boutons associated with characterized spinocervical tract neurons in the cat. Neuroscience 12:151–163

    Google Scholar 

  • Maxwell DJ, Christie WM, Somogyi P (1989) Synaptic connections of GABA-containing boutons in the lateral cervical nucleus of the cat: an ultrastructural study employing pre- and post-embedding immunocytochemical methods. Neuroscience 33:169–184

    Google Scholar 

  • Maxwell DJ, Christie WM, Short AD, Storm-Mathisen J, Ottersen OP (1990 a) Central boutons of glomeruli in the spinal cord of the cat are enriched with L-glutamate-like immunoreactivity. Neuroscience 36:83–104

    Google Scholar 

  • Maxwell DJ, Christie WM, Ottersen OP, Storm-Mathisen J (1990 b) Terminals of group Ia primary afferent fibers in Clarke's column are enriched with L-glutamate-like immunoreactivity. Brain Res 510:346–350

    Google Scholar 

  • Maxwell DJ, Christie WM, Short AD, Brown AG (1991) Direct observations of synapses between GABA-immunoreactive boutons and identified spinocervical tract neurons in the cat's spinal cord. J Comp Neurol 307:375–392

    Google Scholar 

  • Maxwell DJ, Christie WM, Brown AG, Ottersen OP, Storm-Mathisen J (1992) Direct observations of synapses between L-glutamate-immunoreactive boutons and identified spinocervical tract neurones in the spinal cord of the cat. J Comp Neurol 326:485–500

    Google Scholar 

  • Maxwell DJ, Christie WM, Brown AG, Ottersen OP, Storm-Mathisen J (1993) Identified hair follicle afferent boutons in the spinal cord of the cat are enriched with L-glutamate-like immunoreactivity. Brain Res 606:156–161

    Google Scholar 

  • McCarthy PW, Lawson SN (1989) Cell type and conduction velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience 28:745–753

    Google Scholar 

  • McCarthy PW, Lawson SN (1990) Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience 34:623–632

    Google Scholar 

  • McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39:337–388

    Google Scholar 

  • McCormick DA, Krosigk M von (1992) Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proc Natl Acad Sci USA 89:2774–2778

    Google Scholar 

  • McGregor GP, Gibson SJ, Sabate IM, Blank MA, Christofides ND, Wall PD, Polak JM, Bloom SR (1984) Effect of peripheral nerve section and nerve crush on spinal cord neuropeptides in the rat: increased VIP and PHI in the dorsal horn. Neuroscience 13:207–216

    Google Scholar 

  • McLennan H, Huffman RD, Marshall KC (1968) Patterns of excitation of thalamic neurons by amino-acids and by acetylcholine. Nature 219:387–388

    Google Scholar 

  • McMahon SB (1986) The localization of fluoride-resistant acid phosphatase (FRAP) in the pelvic nerves and sacral spinal cord of rats. Neurosci Lett 64:305–310

    Google Scholar 

  • McNeill DL, Chung K, Carlton SM, Coggeshall RE (1988) Calcitonin gene-related peptide immunostained axons provide evidence for fine primary afferent fibers in the dorsal and dorsolateral funiculi of the rat spinal cord. J Comp Neurol 272:303–308

    Google Scholar 

  • McNeill DL, Westlund KN, Coggeshall RE (1989) Peptide immunoreactivity of unmyelinated primary afferent axons in rat lumbar dorsal roots. J Histochem Cytochem 37:1047–1052

    Google Scholar 

  • Menetrey D, Basbaum AI (1987) The distribution of substance P-, enkephalin- and dynorphin-immunoreactive neurons in the medulla of the rat and their contribution to bulbospinal pathways. Neuroscience 23:173–187

    Google Scholar 

  • Mense S (1990) Structure-function relationships in identified neurones. Anat Embryol 181:1–17

    Google Scholar 

  • Merighi A, Polak JM, Fumagalli G, Theodosis DT (1989) Ultrastructural localization of neuropeptides and GABA in rat dorsal horn: a comparison of different immunogold labeling techniques. J Histochem Cytochem 37:529–540

    Google Scholar 

  • Merighi A, Polak JM, Theodosis DT (1991) Ultrastructural visualization of glutamate and aspartate immunoreactivities in the rat dorsal horn, with special reference to the co-localization of glutamate, substance P and calcitonin-gene related peptide. Neuroscience 40:67–80

    Google Scholar 

  • Merighi A, Cruz F, Coimbra A (1992) Immunocytochemical staining of neuropeptides in terminal arborization of primary afferent fibers anterogradely labeled and identified at light and electron microscopic levels. J Neurosci Methods 42:105–113

    Google Scholar 

  • Miletic V, Randic M (1982) Neonatal rat spinal cord slice preparation: postsynaptic effects of neuropeptides on dorsal horn neurons. Dev Brain Res 2:432–438

    Google Scholar 

  • Miletic V, Tan H (1988) Iontophoretic application of calcitonin gene-related peptide produces a slow and prolonged excitation of neurons in the cat lumbar dorsal horn. Brain Res 446:169–172

    Google Scholar 

  • Miletic V, Hoffert MJ, Ruda MA, Dubner R, Shigenaga Y (1984) Serotoninergic axonal contacts on identified cat spinal dorsal horn neurons and their correlation with nucleus raphe magnus stimulation. J Comp Neurol 228:129–141

    Google Scholar 

  • Miller KE, Seybold VS (1987) Comparison of met-enkephalin-, dynorphin A-, and neurotensin-immunoreactive neurons in the cat and rat spinal cords. I. Lumbar cord. J Comp Neurol 255:293–304

    Google Scholar 

  • Molander C, Grant G (1986) Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat. Neuroscience 19:297–312

    Google Scholar 

  • Molander C, Xu Q, Grant G (1984) The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133–141

    Google Scholar 

  • Molander C, Ygge J, Dalsgaard C-J (1987) Substance P-, somatostatin- and calcitonin gene-related peptide-like immunoreactivity and fluoride resistant acid phosphatase activity in relation to retrogradely labelled cutaneous, muscular and visceral primary sensory neurons in the rat. Neurosci Lett 74:37–42

    Google Scholar 

  • Molander C, Xu Q, Rivero-Melian C, Grant G (1989) Cytoarchitectonic organization of the spinal cord in the rat. II. The cervical and upper thoracic cord. J Comp Neurol 289:375–385

    Google Scholar 

  • Molinari M, Hendry SHC, Jones EG (1987) Distributions of certain neuropeptides in the primate thalamus. Brain Res 426:270–289

    Google Scholar 

  • Montero VM (1990) Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons in the cat. Visual Neurosci 4:437–443

    Google Scholar 

  • Montero VM, Wenthold RJ (1989) Quantitative immunogold analysis reveals high glutamate levels in retinal and cortical synaptic terminals in the lateral geniculate nucleus of the macaque. Neuroscience 31:639–647

    Google Scholar 

  • Morris R (1989) Responses of spinal dorsal horn neurones evoked by myelinated primary afferent stimulation are blocked by excitatory amino acid antagonists acting at kainate/quisqualate receptors. Neurosci Lett 105:79–85

    Google Scholar 

  • Mouchet P, Manier M, Feurstein C (1992) Immunohistochemical study of the catecholaminergic innervation of the spinal cord of the rat using specific antibodies against dopamine and noradrenaline. J Chem Neuroanat 5:427–440

    Google Scholar 

  • Murase K, Nedeljkov V, Randic M (1982) The actions of neuropeptides on dorsal horn neurons in rat spinal cord slice preparation: an intracellular study. Brain Res 234:170–176

    Google Scholar 

  • Murase K, Ryu PD, Randic M (1989 a) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103:56–63

    Google Scholar 

  • Murase K, Ryu PD, Randic M (1989 b) Tachykinins modulate multiple ionic conductances in voltage-clamped rat spinal dorsal horn neurons. J Neurophysiol 61:854–865

    Google Scholar 

  • Nagy JI, Hunt SP, Iverson LL, Emson PC (1981) Biochemical and anatomical observations on the degeneration of peptide-containing primary afferent neurons after neonatal capsaicin. Neuroscience 6:1923–1934

    Google Scholar 

  • Nahin RL (1988) Immunocytochemical identification of long ascending, peptidergic lumbar spinal neurons terminating in either the medial or lateral thalamus in the rat. Brain Res 443:345–349

    Google Scholar 

  • Nahin RL, Hylden JLK, Iadarola MJ, Dubner R (1989) Peripheral inflammation is associated with increased dynorphin immunoreactivity in both projection and local circuit neurons in the superficial dorsal horn of the rat lumbar spinal cord. Neurosci Lett 96:247–252

    Google Scholar 

  • Newton BW, Hamill RW (1988) The morphology and distribution of rat serotoninergic intraspinal neurons: an immunohistochemical study. Brain Res Bull 20:349–360

    Google Scholar 

  • Noguchi K, Ruda MA (1992) Gene regulation in an ascending nociceptive pathway: inflammation-induced increase in preprotachykinin mRNA in rat lamina I spinal projection neurons. J Neurosci 12:2563–2572

    Google Scholar 

  • Noguchi K, Morita Y, Kiyama H, Ono K, Tohyama M (1988) A noxious stimulus induces the preprotachykinin-A gene expression in the rat dorsal root ganglion: a quantitative study using in situ hybridization histochemistry. Mol Brain Res 4:31–35

    Google Scholar 

  • Noguchi K, Dubner R, Ruda MA (1992) Preproenkephalin mRNA in spinal dorsal horn neurons is induced by peripheral inflammation and is co-localized with fos and fos-related proteins. Neuroscience 46:561–570

    Google Scholar 

  • Nohr D, Wiehe E, Zentel HJ, Arendt RM (1989) Atrial natriuretic factor-like immunoreactivity in spinal cord and in primary sensory neurons of spinal and trigeminal ganglia of guinea-pig: correlation with tachykinin immunoreactivity. Cell Tissue Res 258:387–392

    Google Scholar 

  • Nothias F, Onteniente B, Roudier F, Peschanski M (1988) Immunocytochemical study of serotoninergic and noradrenergic innervation of the ventrobasal complex of the rat thalamus. Neurosci Lett 95:59–63

    Google Scholar 

  • Nyberg G, Blomqvist A (1985) The somatotopic organization of forelimb cutaneous nerves in the brachial dorsal horn: an anatomical study in the cat. J Comp Neurol 242:28–39

    Google Scholar 

  • O'Brien C, Woolf CJ, Fitzgerald M, Lindsay RM, Molander C (1989) Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience 32:493–502

    Google Scholar 

  • Oertel WH, Graybiel AM, Mugnaini E, Elde RP, Schmechel DE, Kopin IJ (1983) Coexistence of glutamic acid decarboxylase and somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami. J Neurosci 3:1322–1332

    Google Scholar 

  • Ohara PT, Chazal G, Ralston HJ III (1989) Ultrastructural analysis of GABA immunoreactive elements in the monkey thalamic ventrobasal complex. J Comp Neurol 283:541–558

    Google Scholar 

  • Oku R, Satoh M, Fujii N, Otaka A, Yajima H, Takagi H (1987) Calcitonin gene-related peptide promotes mechanical nociception by potentiating release of substance P from the spinal dorsal horn in rats. Brain Res 403:350–354

    Google Scholar 

  • Oku R, Nanayama T, Satoh M (1988) Calcitonin gene-related peptide modulates calcium mobilization in synaptosomes of rat spinal dorsal horn. Brain Res 475:356–360

    Google Scholar 

  • Ositelu DO, Morris R, Vaillant V (1987) Innervation of facial skin but not masticatory muscles or the tongue by trigeminal primary afferents containing somatostatin in the rat. Neurosci Lett 78:271–276

    Google Scholar 

  • Ottersen OP (1987) Postembedding light- and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp Brain Res 69:167–174

    Google Scholar 

  • Ottersen OP (1989 a) Postembedding immunogold labelling of fixed glutamate: an electron microscopic analysis of the relationship between gold particle density and antigen concentration. J Chem Neuroanat 2:57–66

    Google Scholar 

  • Ottersen OP (1989 b) Quantitative electron microscopic immunocytochemistry of neuroactive amino acids. Anat Embryol 180:1–15

    Google Scholar 

  • Ottersen OP (1991) Excitatory amino acid neurotransmitters: anatomical systems. In: Meldrum BS (ed) Excitatory amino acid antagonists. Blackwell, Oxford, pp 14–38

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J (1984 a) Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 229:374–392

    Google Scholar 

  • Ottersen OP, Storm-Mathisen (1984 b) GABA-containing neurons in the thalamus and pretectum of the rodent. An immunocytochemical study. Anat Embryol 170:197–207

    Google Scholar 

  • Ottersen OP, Fischer BO, Storm-Mathisen J (1983) Retrograde transport of D-[3H]aspartate in thalamocortical neurones. Neurosci Lett 42:19–24

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J, Somogyi P (1988) Colocalization of glycine-like and GABA-like immunoreactivities in Golgi cell terminals in the rat cerebellum: a postembedding light and electron microscopic study. Brain Res 450:342–353

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J, Bramham J, Torp R, Laake J, Gundersen V (1990) A quantitative electron microscopic immunocytochemical study of the distribution and synaptic handling of glutamate in rat hippocampus. Prog Brain Res 83:99–114

    Google Scholar 

  • Ottersen OP, Zhang N, Walberg F (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46:519–534

    Article  CAS  PubMed  Google Scholar 

  • Panula P, Yang H-YT, Costa E (1982) Neuronal location of the bombesin-like immunoreactivity in the central nervous system of the rat. Regul Peptides 4:275–283

    Google Scholar 

  • Panula P, Hadjiconstantinou M, Yang H-YT, Costa E (1983) Immunohistochemical localization of bombesin/gastrin-releasing peptide and substance P in primary sensory neurons. J Neurosci 3:2021–2029

    Google Scholar 

  • Panula P, Flügge G, Fuchs E, Pirvola U, Auvinen S, Airaksinen MS (1989) Histamine-immunoreactive fibers in the mammalian spinal cord. Brain Res 484:234–239

    Google Scholar 

  • Patterson JT, Coggeshall RE, Lee WT, Chung K (1990) Long ascending unmyelinated primary afferent axons in the rat dorsal column: immunohistochemical localizations. Neurosci Lett 108:6–10

    Google Scholar 

  • Pearson JC, Goldfinger MD (1987) The morphology and distribution of serotonin-like immunoreactive fibers in the cat dorsal column nuclei. Neurosci Lett 74:125–131

    Google Scholar 

  • Penn RD, Paice JA, Kroin JS (1990) Intrathecal octreotide for cancer pain. Lancet 335:738

    Google Scholar 

  • Penny GR, Fitzpatrick D, Schmechel DE, Diamond IT (1983) Glutamic acid decarboxylase-immunoreactive neurons and horseradish peroxidase-labeled projection neurons in the ventral posterior nucleus of the cat and Galago senegalensis. J Neurosci 3:1868–1887

    Google Scholar 

  • Phend KD, Weinberg RJ, Valtschanoff JG, Rustioni A (1992) Amino acid immunocytochemistry of primary afferent terminals in deep laminae of the rat dorsal horn. Soc Neurosci Abstr 18:1150

    Google Scholar 

  • Plantinga LC, Verhaagen J, Edwards PM, Schrama LH, Burbach JPH, Gispen WH (1992) Expression of the pro-opiomelanocortin gene in dorsal root ganglia, spinal cord and sciatic nerve after sciatic nerve crush in the rat. Mol Brain Res 16:135–142

    Google Scholar 

  • Potashner SJ, Tran PL (1984) Decreased uptake and release of D-aspartate in the guinea-pig spinal cord after dorsal root section. J Neurochem 42:1135–1144

    Google Scholar 

  • Potashner SJ, Dymczyk L, Deangelis MM (1988) D-Aspartate uptake and release in the guinea-pig spinal cord after partial ablation of the cerebral cortex. J Neurochem 50:103–111

    Google Scholar 

  • Pourcho RG, Goebel DJ, Jojich L, Hazlett JC (1992) Immunocytochemical evidence for the involvement of glycine in sensory centers of the rat brain. Neuroscience 46:643–656

    Google Scholar 

  • Powell JJ, Todd AJ (1992) Light and electron microscope study of GABA-immunoreactive neurons in lamina III of rat spinal cord. J Comp Neurol 315:125–136

    Google Scholar 

  • Pritz MB, Stritzel ME (1989) Reptilian dorsal column nucleus lacks GAD immunoreactive neurons. Brain Res 503:175–179

    Google Scholar 

  • Rajaofetra N, Ridet J-L, Poulat P, Marlier L, Sandillon F, Geffard M, Privat A (1992) Immunocytochemical mapping of noradrenergic projections to the rat spinal cord with an antiserum against noradrenaline. J Neurocytol 21:481–494

    Google Scholar 

  • Ralston HJ (1979) The fine structure of laminae I, II and III of the macaque spinal cord. J Comp Neurol 184:619–642

    Google Scholar 

  • Ralston HJ III (1991) Local circuitry of the somatosensory thalamus in the processing of sensory information. Brain Res 87:13–28

    Google Scholar 

  • Ralston HJ III, Ralston DD (1992 a) The primate dorsal spinothalamic tract: evidence for a specific termination in the posterior nuclei (Po/SG) of the thalamus. Pain 48:107–118

    Google Scholar 

  • Ralston DD, Ralston HJ III (1992 b) Spinothalamic tract terminals in M. fascicularis: 3-dimensional computer-assisted reconstructions of synaptic relationships. Soc Neurosci Abstr 18:1018

    Google Scholar 

  • Randic M, Miletic V (1978) Depressaut actions of methionine-enkephalin and somatostatin in cat dorsal horn neurones activated by noxious stimuli. Brain Res 152:196–202

    Google Scholar 

  • Randic M, Gerber G, Ryu PD, Kangrga I (1987) Inhibitory actions of galanin and somatostatin 28 on rat spinal dorsal horn neurons. Soc Neurosci Abstr 13:1308

    Google Scholar 

  • Randic M, Hecimovic H, Ryu PD (1990) Substance P modulates glutamate-induced currents in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 117:74–80

    Google Scholar 

  • Rexed B (1952) The cytoarchitechtonic organization of the spinal cord in the cat. J Comp Neurol 96:415–496

    Google Scholar 

  • Ribeiro-da-Silva A, Cuello AC (1990) Choline acetyltransferase-immunoreactive profiles are presynaptic to primary sensory fibers in the rat superficial dorsal horn. J Comp Neurol 295:370–384

    Google Scholar 

  • Ribeiro-da-Silva A, Pioro EP, Cuello AC (1991) Substance P- and enkephalin-like immunoreactivities are colocalized in certain neurons of the substantia gelatinosa of the rat spinal cord: an ultrastructural double-labeling study. J Neurosci 11:1068–1080

    Google Scholar 

  • Ribeiro-da-Silva A, Ballak M, Cuello AC (1993) GABA immunoreactivity is co-localized with enkephalin or ChAT immunoreactivities in the dorsal horn of the rat spinal cord. An ultrastructural double-labeling study. Soc Neurosci Abstr 19:1196

    Google Scholar 

  • Rinvik E, Ottersen OP, Storm-Mathisen J (1987) Gamma-aminobutyrate-like immunoreactivity in the thalamus of the cat. Neuroscience 21:781–805

    Google Scholar 

  • Rivero-Melian C, Grant G (1990) Distribution of lumbar dorsal root fibers in the lower thoracic and lumbosacral spinal cord of the rat studied with choleragenoid horseradish peroxidase conjugate. J Comp Neurol 299:470–481

    Google Scholar 

  • Roberts F, Hill RG (1978) The effect of dorsal column lesions on amino acid levels and glutamate uptake in rat dorsal column nuclei. J Neurochem 31:1549–1551

    Google Scholar 

  • Roberts PJ (1974) The release of amino acids with proposed neurotransmitter function from the cuneate and gracile nuclei of the rat in vivo. Brain Res 67:419–428

    Google Scholar 

  • Roberts PJ, Mitchell JF (1972) The release of amino acids from the hemisected spinal cord during stimulation. J Neurochem 19:2473–2482

    Google Scholar 

  • Roberts PJ, Keen P, Mitchell JF (1973) The distribution and axonal transport of free amino acids and related compounds in the dorsal sensory neuron of the rat, as determined by the dansyl reaction. J Neurochem 21:199–209

    Google Scholar 

  • Robertson B, Grant G (1985) A comparison between wheat germ agglutinin- and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat. Neuroscience 14:895–905

    Google Scholar 

  • Roettger VR, Pearson JC, Goldfinger MD (1989) Identification of γ-aminobutyric acid-like immunoreactive neurons in the rat cuneate nucleus. Neurosci Lett 97:46–50

    Google Scholar 

  • Rosenfeld MG, Mermod J-J, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evand RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene with tissue-specific RNA processing. Nature 304:129–135

    Google Scholar 

  • Ross CA, Armstrong DM, Ruggiero DA, Pickel VM, Job TH, Reis DJ (1981) Adrenaline neurons in the rostral ventrolateral medulla innervate thoracic spinal cord: a combined immunocytochemical and retrograde transport demonstration. Neurosci Lett 25:257–262

    Google Scholar 

  • Rousselot P, Papadopoulos G, Merighi A, Poulain DA, Theodosis DT (1990) Oxytocinergic innervation of the rat spinal cord. An electron microscopic study. Brain Res 529:178–184

    Google Scholar 

  • Ruda MA (1982) Opiates and pain pathways: demonstration of enkephalin synapses on dorsal horn projection neurons. Science 215:1523–1525

    Google Scholar 

  • Ruda MA, Coffield J, Steinbusch HWM (1982) Immunocytochemical analysis of serotonergic axons in laminae I and II of the lumbar spinal cord of the cat. J Neurosci 2:1660–1671

    CAS  PubMed  Google Scholar 

  • Ruda MA, Coffield J, Bennett GJ, Dubner R (1983) Role of serotonin (5-HT) and enkephalin (ENK) in trigeminal and spinal pain pathways. J Dent Res 62:691

    Google Scholar 

  • Ruda MA, Coffield J, Dubner R (1984) Demonstration of postsynaptic opioid modulation of thalamic projection neurons by the combined techniques of retrograde horseradish peroxidase and enkephalin immunocytochemistry. J Neurosci 4:2117–2132

    Google Scholar 

  • Ruda MA, Bennett GJ, Dubner R (1986) Neurochemistry and neural circuitry in the dorsal horn. Prog Brain Res 66:219–268

    Google Scholar 

  • Rustioni A, Cuénod M (1982) Selective retrograde transport of D- aspartate in spinal interneurons and cortical neurons of rats. Brain Res 236:143–155

    Google Scholar 

  • Rustioni A, Weinberg RJ (1989) The somatosensory system. In: Björklund A, Hökfelt T, Swanson LW (eds) Handbook of chemical neuroanatomy, vol 7. Elsevier, Amsterdam, pp 219–321

    Google Scholar 

  • Rustioni A, Schmechel DE, Spreafico R, Cheema S, Cuénod M (1983) Excitatory and inhibitory amino-acid putative neurotransmitters in the ventralis posterior complex: an autoradiographic and immunocytochemical study in rats and cats. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory integration in the thalamus. Elsevier, Amsterdam, pp 365–383

    Google Scholar 

  • Rustioni A, Schmechel DE, Cheema S, Fitzpatrick D (1984) Glutamic acid decarboxylase-containing neurons in the dorsal column nuclei of the cat. Somatosens Res 1:329–357

    Google Scholar 

  • Ryu PD, Gerber G, Murase K, Randic M (1988) Actions of calcitonin gene-related peptide on rat spinal dorsal horn neurons. Brain Res 441:357–361

    Google Scholar 

  • Salt TE (1986) Mediation of thalamic sensory input by both NM-DA receptors and non-NMDA receptors. Nature 322:263–265

    Google Scholar 

  • Salt TE, Eaton SA (1989) Function of non-NMDA receptors and NMDA receptors in synaptic responses to natural somatosensory stimulation in the ventrobasal thalamus. Exp Brain Res 77:646–652

    Google Scholar 

  • Salt TE, Eaton SA (1991) Sensory excitatory postsynaptic potentials mediated by NMDA and non-NMDA receptors in the thalamus in vivo. Eur J Neurosci 3:296–300

    Google Scholar 

  • Salt TE, Hill RG (1983) Neurotransmitter candidates of somatosensory primary afferent fibers. Neuroscience 10:1083–1103

    Google Scholar 

  • Salter MW, Henry JL (1985) Effects of adenosine 5′-monophosphate and adenosine 5′-triphosphate on functionally identified units in the cat spinal dorsal horn. Evidence for a differential effect of adenosine 5′-triphosphate on nociceptive vs non-nociceptive units. Neuroscience 15:815–825

    Google Scholar 

  • Salter MW, Henry JL (1991) Responses of functionally identified neurones in the dorsal horn of the cat spinal cord to substance P, neurokinin A and physalaemin. Neuroscience 43:601–610

    Google Scholar 

  • Saper CB, Hurley KM, Moga MM, Holmes HR, Adams SA, Leahy KM, Needleman P (1989) Brain natriuretic peptides: differential localization of a new family of neuropeptides. Neurosci Lett 96:29–34

    Google Scholar 

  • Sastry BR (1979) Presynaptic effects of morphine and methionine-enkephalin in feline spinal cord. Neuropharmacology 18:367–375

    Google Scholar 

  • Sawynok J, Sweeney ME (1989) The role of purines in nociception. Neuroscience 32:557–569

    Google Scholar 

  • Schneider SP, Perl ER (1985) Selective excitation of neurons in the mammalian spinal dorsal horn by aspartate and glutamate in vitro: correlation with location and excitatory input. Brain Res 360:339–343

    Google Scholar 

  • Schneider SP, Perl ER (1988) Comparison of primary afferent and glutamate excitation of neurons in the mammalian spinal dorsal horn. J Neurosci 8:2062–2073

    Google Scholar 

  • Schouenborg J, Sjölund BH (1986) First-order nociceptive synapses in rat dorsal horn are blocked by amino acid antagonists. Brain Res 379:394–398

    Google Scholar 

  • Senba E, Shiosaka S, Hava Y, Inagaki S, Sakanaka M, Takatsuki K, Kawai Y, Tahyama M (1982) Ontogeny of the peptidergic system in the rat spinal cord: immunohistochemical analysis. J Comp Neurol 208:54–66

    Google Scholar 

  • Seroogy KB, Mohapatra NK, Lund PK, Réthelyi M, McGehee DS, Perl ER (1990) Species-specific expression of cholecystokinin messenger RNA in rodent dorsal root ganglia. Mol Brain Res 7:171–176

    Google Scholar 

  • Serrano LP, Craig AD (1992) Effects of systemic morphine on lamina I neurons in the cat. Soc Neurosci Abstr 18:1023

    Google Scholar 

  • Seybold VS, Elde RP (1980) Immunohistochemical studies of peptidergic neurons in the dorsal horn of the spinal cord. J Histochem Cytochem 28:367–370

    Google Scholar 

  • Seybold VS, Elde RP (1982) Neurotensin immunoreactivity in the superficial laminae of the dorsal horn of the rat. I. Light microscope studies of cell bodies and proximal dendrites. J Comp Neurol 205:89–100

    Google Scholar 

  • Shehab SAS, Atkinson ME (1986) Vasoactive intestinal polypeptide (VIP) increases in the spinal cord after peripheral axotomy of the sciatic nerve originate from primary afferent neurons. Brain Res 372:37–44

    Google Scholar 

  • Simone DA, Pubols BH Jr (1991) The raccoon lateral cervical nucleus: a single-unit analysis. J Neurophysiol 65:1411–1421

    Google Scholar 

  • Skilling SR, Smullin DH, Larson AA (1988) Extracellular amino acid concentrations in the dorsal spinal cord of freely moving rats following veratridine and nociceptive stimulation. J Neurochem 51:127–132

    Google Scholar 

  • Skilling SR, Smullin DH, Larson AA (1990) Differential effects of C- and N-terminal substance P metabolites on the release of amino acid neurotransmitters from the spinal cord: potential role in nociception. J Neurosci 10:1309–1318

    Google Scholar 

  • Skofitsch G, Zamir N, Helke C, Savitt J, Jacobowitz D (1985) Corticotropin releasing factor-like immunoreactivity in sensory ganglia and capsaicin sensitive neurons of the rat central nervous system: colocalization with other neuropeptides. Peptides 6:307–318

    Google Scholar 

  • Sluka KA, Westlund KN (1992) Spinal projections of the locus coeruleus and the nucleus subcoeruleus in the Harlan and the Sasco Sprague-Dawley rat. Brain Res 579:67–73

    Google Scholar 

  • Sluka KA, Dougherty PM, Sorkin LS, Willis WD, Westlund KN (1992) Neural changes in acute arthritis in monkeys. III. Changes in substance P, calcitonin gene-related peptide and glutamate in the dorsal horn of the spinal cord. Brain Res Rev 17:29–38

    Google Scholar 

  • Smith GD, Harmar AJ, McQueen DS, Seckl JR (1992) Increase in substance P and CGRP, but not somatostatin content of innervating dorsal root ganglia in adjuvant monoarthritis in the rat. Neurosci Lett 137:257–260

    Google Scholar 

  • Smith Y, Séguéla P, Parent A (1987) Distribution of GABA-immunoreactive neurons in the thalamus of the squirrel monkey (Saimiri sciureus). Neuroscience 22:579–591

    Google Scholar 

  • Smullin DH, Skilling SR, Larson AA (1990) Interactions between substance P, calcitonin gene-related peptide, taurine and excitatory amino acids in the spinal cord. Pain 42:93–101

    Google Scholar 

  • Somogyi P, Hodgson AJ (1985) Antisera to γ-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249–257

    Google Scholar 

  • Somogyi P, Halasy K, Somogyi J, Storm-Mathisen J, Ottersen OP (1986) Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19:1045–1050

    Google Scholar 

  • Spreafico R, Schmechel DE, Ellis LC Jr, Rustioni A (1983) Cortical relay neurons and interneurons in the n. ventralis posterolateralis of cats: a horseradish peroxidase, electron-microscopic, Golgi and immunocytochemical study. Neuroscience 9:491–509

    Google Scholar 

  • Steinbusch HWM (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat — cell bodies and terminals. Neuroscience 6:557–618

    Google Scholar 

  • Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742

    Google Scholar 

  • Steriade M, Paré D, Parent A, Smith Y (1988) Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey. Neuroscience 25:47–67

    Google Scholar 

  • Storm-Mathisen J, Ottersen OP (1988) Anatomy of putative glutamatergic neurons. In: Avoli M, Reader TA, Dykes RW, Gloor P (eds) Neurotransmitters and cortical function. Plenum Press, New York, pp 39–70

    Google Scholar 

  • Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug F-MS, Ottersen OP (1983) First visualization of glutamate and GABA in neurons by immunocytochemistry. Nature 301:517–520

    Google Scholar 

  • Suzue T, Jessel T (1980) Opiate analgesics and endorphins inhibit rat dorsal root potential in vitro. Neurosci Lett 16:161–166

    Google Scholar 

  • Svensson BA, Rastad J, Westman J, Wiberg M (1985) Somatotopic termination of spinal afferents to the feline lateral cervical nucleus. Exp Brain Res 57:576–584

    Google Scholar 

  • Svensson BA, Griph S, Rastad J, Westman J (1987) Quantitative ultrastructural study of boutons of ascending afferents to the feline lateral cervical nucleus. Brain Res 423:229–236

    Google Scholar 

  • Swaab DF, Visser B (1977) Immunohistochemical localization of a-melanocyte stimulating hormone (α-MSH)-like compounds in the rat nervous system. Neurosci Lett 7:313–317

    Google Scholar 

  • Tamatani M, Senba E, Tohyama M (1989) Calcitonin gene-related peptide- and substance P-containing primary afferent fibers in the dorsal column of the rat. Brain Res 495:122–130

    Google Scholar 

  • Tashiro T, Takahashi O, Satoda T, Matsushima R, Mizuno N (1987) Immunohistochemical demonstration of coexistence of enkephalin- and substance P-like immunoreactivities in axonal components in the lumbar segments of cat spinal cord. Brain Res 424:391–395

    Google Scholar 

  • Tashiro T, Satoda T, Takahashi O, Matsushima R, Mizuno N (1988) Distribution of axons exhibiting both enkephalin- and serotonin-like immunoreactivities in the lumbar cord segments: an immunohistochemical study in the cat. Brain Res 440:357–362

    Google Scholar 

  • Tashiro T, Ruda MA, Satoda T, Matsushima R, Mizuno N (1989) Convergence of serotonin-, enkephalin- and substance P-like immunoreactive afferent fibers onto cat medullary dorsal horn projection neurons: a triple immunocytochemical staining technique combined with the retrograde HRP-tracing method. Brain Res 491:360–365

    Google Scholar 

  • Todd AJ (1990) An electron microscope study of glycine-like immunoreactivity in laminae I–III of the spinal dorsal horn of the rat. Neuroscience 39:387–394

    Google Scholar 

  • Todd AJ (1991) Immunohistochemical evidence that acetylcholine and glycine exist in different populations of GABAergic neurons in lamina III of rat spinal dorsal horn. Neuroscience 44:741–746

    Google Scholar 

  • Todd AJ, Sullivan AG (1990) Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296:496–505

    Google Scholar 

  • Todd AJ, Maxwell DJ, Brown AG (1991) Relationships beween hair-follicle afferent axons and glycine-immunoreactive profiles in cat spinal dorsal horn. Brain Res 564:132–137

    Google Scholar 

  • Tracey DJ, De Biasi S, Phend K, Rustioni A (1991) Aspartate-like immunoreactivity in primary afferent neurons. Neuroscience 40:673–686

    Google Scholar 

  • Valtschanoff J, Weinberg RJ, Rustioni A (1991) Immunolabeling of terminals of cortical descending fibers. Soc Neurosci Abstr 17:258

    Google Scholar 

  • Valtschanoff JG, Weinberg RJ, Rustioni A (1993) Amino acid immunoreactivity in corticospinal terminals. Exp Brain Res 93:95–103

    Google Scholar 

  • Verge VMK, Wiesenfeld-Hallin Z, Hökfelt T (1993) Cholecystokinin in mammalian primary sensory neurons and spinal cord: in situ hybridization studies in rat and monkey. Eur J Neurosci 5:240–250

    Google Scholar 

  • Villar MJ, Cortés R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, Emson PC, Hökfelt T (1989) Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33:587–604

    Google Scholar 

  • Villar MJ, Wiesenfeld-Hallin Z, Xu X-J, Theodorsson E, Emson PC, Hökfelt T (1991) Further studies on galanin-, substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: effects of dorsal rhizotomies and sciatic nerve lesions. Exp Neurol 112:29–39

    Google Scholar 

  • Vincent SR, Hökfelt T, Christensson I, Terenius L (1982) Dynorphin-immunoreactive neurons in the central nervous system of the rat. Neurosci Lett 33:185–190

    Google Scholar 

  • Wahlestedt C, Skagerberg G, Hakanson R, Sundler F, Wada H, Watanabe T (1985) Spinal projections of hypothalamic histidine decarboxylase-immunoreactive neurones. Agents Actions 16:231–233

    Google Scholar 

  • Wall PD (1967) The laminar organization of the dorsal horn and effects of descending impulses. J Physiol (Lond) 188:403–423

    Google Scholar 

  • Walmsley B, Nicol MJ (1991) The effects of Ca2+, Mg2+ and kynurenate on primary afferent synaptic potentials evoked in cat spinal cord neurones in vivo. J Physiol (Lond) 433:409–420

    Google Scholar 

  • Weihe E, Hartschuh W, Weber E (1985) Prodynorphin opioid peptides in small somatosensory primary afferents of guinea-pig. Neurosci Lett 58:347–352

    Google Scholar 

  • Weinberg RJ, Rustioni A (1989) Brainstem projections to the rat cuneate nucleus. J Comp Neurol 282:142–156

    Google Scholar 

  • Westlund KN, Carlton SM, Zhang D, Willis WD (1990 a) Direct catecholaminergic innervation of primate spinothalamic tract neurons. J Comp Neurol 299:178–186

    Google Scholar 

  • Westlund KN, Sorkin LS, Ferrington DG, Carlton SM, Willcockson HH, Willis WD (1990 b) Serotoninergic and noradrenergic projections to the ventral posterolateral nucleus of the monkey thalamus. J Comp Neurol 295:197–207

    Google Scholar 

  • Westlund KN, Carlton SM, Zhang D, Willis WD (1992) Glutamate-immunoreactive terminals synapse on primate spinothalamic tract cells. J Comp Neurol 322:519–527

    Google Scholar 

  • Westman J (1968) The lateral cervical nucleus in the cat. I. A Golgi study. Brain Res 10:352–368

    Google Scholar 

  • Westman J, Blomqvist A, Köhler C, Wu J-Y (1984) Light and electron microscopic localization of glutamic acid decarboxylase and substance P in the dorsal column nuclei of the cat. Neurosci Lett 51:347–352

    Google Scholar 

  • White TD, Downie JW, Leslie RA (1985) Characteristics of K+- and veratridine-induced release of ATP from synaptosomes prepared from dorsal and ventral spinal cord. Brain Res 334:372–374

    Google Scholar 

  • Wiberg M, Westman J, Blomqvist A (1987) Somatosensory projection to the mesencephalon: an anatomical study in the monkey. J Comp Neurol 264:92–117

    Google Scholar 

  • Wiesenfeld-Hallin Z, Villar MJ, Hökfelt T (1989) The effects of intrathecal galanin and C-fiber stimulation on the flexor reflex in the rat. Brain Res 486:205–213

    Google Scholar 

  • Wiesenfeld-Hallin Z, Xu X-J, Langel Ü, Bedecs K, Hökfelt T, Bartfai T (1992) Galanin-mediated control of pain: enhanced role after nerve injury. Proc Natl Acad Sci USA 89:3334–3337

    Google Scholar 

  • Willcockson HH, Carlton SM, Willis WD (1987) Mapping study of serotoninergic input to diencephalic-projecting dorsal column neurons in the rat. J Comp Neurol 261:467–480

    Google Scholar 

  • Willcockson WS, Chung JM, Hori Y, Lee KH, Willis WD (1984) Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J Neurosci 4:732–740

    CAS  PubMed  Google Scholar 

  • Willis WD Jr, Coggeshall RE (1991) Sensory mechanisms of the spinal cord, 2nd ed. Plenum Press, New York

    Google Scholar 

  • Yamazoe M, Shiosaka S, Yagura A, Kawai Y, Shibasaki T, Ling N, Tohyama M (1984) The distribution of α-melanocyte stimulating hormone (αMSH) in the central nervous system of the rat: an immunohistochemical study. II. Lower brain stem. Peptides 5:721–727

    Google Scholar 

  • Yanagisawa M, Yagi N, Otsuka M, Yanaihara C, Yanaihara N (1986) Inhibitory effects of galanin on the isolated spinal cord of the newborn rat. Neurosci Lett 70:278–282

    Google Scholar 

  • Ygge J, Grant G (1983) The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglionic transport of horseradish peroxidase. J Comp Neurol 216:1–9

    Google Scholar 

  • Yoshida A, Dostrovsky JO, Chiang CY (1992) The afferent and efferent connections of the nucleus submedius in the rat. J Comp Neurol 324:115–133

    Google Scholar 

  • Yoshida M, Tanaka M (1988) Existence of a new dopaminergic terminal plexus in the rat spinal cord: assessment by immunohistochemistry using anti-dopamine serum. Neurosci Lett 94:5–9

    Google Scholar 

  • Yoshimura M, Jessel T (1990) Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J Physiol (Lond) 430:315–335

    Google Scholar 

  • Yoshimura M, Nishi S (1992) Excitatory amino acid receptors involved in primary afferent-evoked polysynaptic EPSPs of substantia gelatinosa neurons in the adult rat spinal cord slice. Neurosci Lett 143:131–134

    Google Scholar 

  • Yoshimura M, Murase K, Arancio O, MacDermott AB (1991) Glutamate receptor agonist-induced inward currents in spinal dorsal horn neurons dissociated from the adult rat. Neurosci Res 12:528–535

    Google Scholar 

  • Yoshioka K, Jessel TM (1984) ATP release from the dorsal horn of the rat spinal cord. Soc Neurosci Abstr 10:993

    Google Scholar 

  • Young AB, Bromberg MB, Penney JB Jr (1981) Decreased glutamate uptake in subcortical areas deafferented by sensorimotor cortical ablation in the cat. J Neurosci 1:241–249

    Google Scholar 

  • Zhang D, Owens CM, Willis WD (1991) Short-latency excitatory postsynaptic potentials are evoked in primate spinothalamic tract neurons by corticospinal tract volleys. Pain 45:197–201

    Google Scholar 

  • Zhang N, Ottersen OP (1992) Differential cellular distribution of two sulphur-containing amino acids in rat cerebellum. An immunocytochemical investigation using antisera to taurine and homocysteic acid. Exp Brain Res 90:11–20

    Google Scholar 

  • Zieglgänzberger W, Herz A (1971) Changes of cutaneous receptive fields of spino-cervical-tract neurones and other dorsal horn neurones by microelectrophoretically administered amino acids. Exp Brain Res 13:111–126

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Broman, J. Neurotransmitters in subcortical somatosensory pathways. Anat Embryol 189, 181–214 (1994). https://doi.org/10.1007/BF00239008

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239008

Key words

Navigation