Skip to main content

Transsynaptic induction of c-fos in basal forebrain, diencephalic and midbrain neurons following AMPA-induced activation of the dorsal and ventral striatum

Experimental Brain Research volume 93, pages 399–411 (1993)Cite this article

Abstract

In these experiments, induction of the immediate early gene c-fos following excitation of striatal neurons has been used to investigate the organization of the ventral and dorsal striatopallidal systems and the relationship between striatal neurons and cholinergic neurons of the nucleus basalis magnocellularis (of Meynert, nbM). The results demonstrate that FOS immunoreactivity (ir) can be detected in ventral and dorsal striatal neurons following infusions of the non-N-methyl-d-aspartic acid (NMDA) glutamate receptor agonist α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA). This activation and increased expression of FOS in striatal neurons was itself associated with the sustained appearance of FOS-ir in neurons of the ipsilateral ventral and dorsal pallidum, subthalamic nucleus and some thalamic nuclei. Infusions of AMPA into the ventral striatum (VS), but not the dorsal striatum (DS), also resulted in the appearance of FOS-ir in a proportion (17%) of the cholinergic neurons of the nbM. By combining the retrograde transport of Fluoro-Gold with FOS immunocytochemistry, it was also possible to demonstrate that approximately 46% and 58% of the pallidal neurons containing FOS-ir after infusions of AMPA into the VS or DS, respectively, directly project to the subthalamic nucleus. Taken together, these observations suggest that visualizing the protein product of transsynaptic c-fos induction provides an effective way to study the topographic and transsynaptic, within-system consequences of striatal activation.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Albin RL, Makowiec RL, Hollingsworth ZR, Dure IV LS, Penney JB, Young AB (1992) Excitatory amino acid binding sites in the basal ganglia of the rat: a quantitative autoradiographic study. Neuroscience 46:35–48

    Google Scholar 

  • Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid and corticopetal components of the substantia innominata. Neuroscience 27:1–39

    Google Scholar 

  • Arnold FJL, M de Lucas Bueno, H Shiers, DC Hancock, GI Evan and J Herbert (1992) Expression of c-fos in regions of the basal limbic forebrain following intracerebroventricular corticotrophin-releasing factor (CRF) in unstressed or stressed male rats. Neuroscience 51:377–390

    Google Scholar 

  • Barbeito L, Cheramy A, Godeheu G, Desce JM, Glowinski J (1990) Glutamate receptors of a quisqualate-kainate subtype are involved in the presynaptic regulation of dopamine release in the cat caudate nucleus in vivo. Eur J Neurosci 2:304–311

    Google Scholar 

  • Baum MJ, Everitt BJ (1992) Increased expression of c-fos in the medial preoptic area after mating in the male rat: role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience 50:627–646

    Google Scholar 

  • Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline and pentylenetetrazol: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6:1361–1391

    Article  CAS  PubMed  Google Scholar 

  • Berendse HW, Groenewegen HJ (1991) The connections of the medial part of the subthalamic nucleus in the rat: evidence for a parallel organization. In: Bernardi G (ed) The basal ganglia III. Plenum, Nem York, pp 89–98

    Google Scholar 

  • Bigl V, Woolf NJ, Butcher LL (1982) Cholinergic projection from the basal forebrain to frontal, parietal, temporal, occipital and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 8:727–749

    Google Scholar 

  • Bullitt E (1990) Expression of c-foc-like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol 296:517–530

    Google Scholar 

  • Burns LH, Everitt BJ, Robbing TW (1991) Functional interactions of limbic afferents to the ventral striatum with mesolimbic dopamine: studies of conditioned reinforcement and locomotor activity in the rat. Soc Neurosci Abstr 17(1): 494.6

    Google Scholar 

  • Carlsen J, Zaborszky L, Heimer L (1985) Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 234:155–167

    Google Scholar 

  • Carlsson M, Carlsson A (1990) Interactions between glutamatergic and monoaminergic systems within the basal ganglia — implications for schizophrenia and Parkinson's disease. Trends Neurosci 13:272–276

    Google Scholar 

  • Cenci MA, Campbell K, Wictorin K, Björklund A (1992) Striatal c-fos induction by cocaine or apomorphine occurs preferentially in output neurons projecting to the substantia nigra in the rat. Eur J Neurosci 4:376–380

    Google Scholar 

  • Clow DW, Jhamandas K (1989) Characterization of l-glutamate action on the release of endogenous dopamine from the rat caudate-putamen. J Pharmacol Exp Ther 248:722–728

    Google Scholar 

  • Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474–476

    Google Scholar 

  • Cornwall J, Phillipson OT (1988) Afferent projections to the dorsal thalamus of the rat as shown by retrograde lectin transport -I. The mediodorsal nucleus. Neuroscience 24:1035–1049

    Google Scholar 

  • Cullinan WE, Zaborszky L (1991) Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of Cholinergic projection neurons. J Comp Neurol 306:631–667

    Google Scholar 

  • Curran T, Franza RB Jr (1988) Fos and Jun: the AP1 connection. Cell 55:395–397

    Google Scholar 

  • Curran T, Morgan JI (1987) Memories of fos. Bioessays 7(6): 255–258

    Google Scholar 

  • Deutch AY, Cameron DS (1992) Pharmacological comparison of dopamine systems in the nucleus accumbens core and shell. Neuroscience 46:49–56

    Google Scholar 

  • Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261–265

    Google Scholar 

  • Dragunow M, Robertson HA (1987) Kindling stimulation induces c-fos protein in granule cells of the rat dentate gyrus. Nature 329:441

    Google Scholar 

  • Dragunow M, Robertson HA (1988) Localization and induction of c-fos protein-like immunoreactive material in the nuclei of adult mammalian neurons. Brain Res 440:252–260

    Google Scholar 

  • Dragunow M, Robertson GS, Faull RLM, Robertson HA, Jansen K (1990) D2 dopamine receptor antagonists induce Fos and related proteins in rat striatal neurons. Neuroscience 37:287–294

    Google Scholar 

  • Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267:455–471

    Google Scholar 

  • Dudchenko P, Sarter M (1991) GABAergic control of basal forebrain Cholinergic neurons and memory. Behav Brain Res 42:33–41

    Google Scholar 

  • Dunnett SB (1985) Comparative effects of Cholinergic drugs and lesions of nucleus basalis or fimbria-fornix on delayed matching in rats. Psychopharmacology 87:357–363

    Google Scholar 

  • Dunnett SB, Everitt BJ, Robbins TW (1991) The basal forebraincortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci 14(11): 494–500

    Google Scholar 

  • Everitt BJ, Robbins JL, Evenden JL, Marston HM, Jones GH, Sirkiä TE (1987) The effects of excitotoxic lesions of the substantia innominata, ventral and dorsal globus pallidus on the acquisition and retention of a conditional visual discrimination: implications for cholinergic hypotheses of learning and memory. Neuroscience 22:441–469

    Google Scholar 

  • Everitt BJ, Sirkiä TE, Roberts AC, Jones GH, Robbins TW (1988) Distribution and some projections of cholinergic neurons in the brain of the common marmoset, Callithrix jacchus. J Comp Neurol 271:533–558

    Google Scholar 

  • Fitzgerald M (1990) c-Fos and the changing face of pain. Trends Neurosci 13:439–440

    Google Scholar 

  • Fuxe K, Agnati LF, Rosen L, Bjelke B, Cintra A, Bortolotti F, Tinner B, Andersson C, Hasselroth U, Steinbusch H (1991) Computer-assisted image analysis techniques allow a characterization of the compartments within the basal ganglia. Focus on functional compartments produced by d-amphetamine activation of the c-fos gene and its relationship to the glucocorticoid receptor. J Chem Neuroanat 4:355–372

    Google Scholar 

  • le Gal la Salle G (1988) Long-lasting and sequential increase of c-fos oncoprotein expression in kainate-induced status epilepticus. Neurosci Lett 88:127–130

    Google Scholar 

  • Garthwaite G, Garthwaite J (1989) Differential dependence on Ca2+ of N-methyl-d-aspartate and quisqualate neurotoxicity in young rat hippocampal slices. Neurosci Lett 97:316–322

    Google Scholar 

  • Garthwaite G, Williams GD, Garthwaite J (1992) Glutamate toxicity: an experimental and theoretical analysis. Eur J Neurosci 4:353–360

    Google Scholar 

  • Gaykema RPA, Weeghel R van, Hersh LB, Luiten PGM (1991) Prefrontal cortical projections to the cholinergic neurons in the basal forebrain. J Comp Neurol 303:563–583

    Google Scholar 

  • Gerfen CR (1989) The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246:385–388

    Google Scholar 

  • Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15:133–139

    Google Scholar 

  • Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ, Sibley DR (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250:1429–1432

    CAS  PubMed  Google Scholar 

  • Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13:244–254

    Google Scholar 

  • Graybiel AM, Moratalla R, Robertson HA (1990) Amphetamine and cocaine induce drug-specific activation of c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc Natl Acad Sci USA 87:6912–6916

    Google Scholar 

  • Groenewegen HJ, Berendse HW (1990) Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol 294:607–622

    CAS  PubMed  Google Scholar 

  • Groenewegen HJ, Meredith GE, Berendse HW, Voorn P, Wolters JG (1989) The compartmental organization of the ventral striatum in the rat. In: Grossman, Sambrook (eds) Neural basis for disorders in movement. Libbey, London, pp 45–54

    Google Scholar 

  • Groenewegen HJ, Berendse HW, Wolters JG, Lohman AHM (1990) The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. Prog Brain Res 85:95–118

    Google Scholar 

  • Groenewegen HJ, Berendse HW, Meredith GE, Haber SN, Voorn P, Wolters JG, Lohman AHM (1991) Functional anatomy of the ventral, limbic system-innervated striatum. In: Willner P, Scheel-Kruger J (eds) The mesolimbic dopamine system: from motivation to action. Wiley, Chichester, pp 19–60

    Google Scholar 

  • Grove EA, Domesick VB, Nauta WJH (1986) Light microscopic evidence of a striatal input to intrapallidal neurons of cholinergic cell group Ch4:a study employing the anterograde tracer Phaseolus leucoagglutinin (PHA-L). Brain Res 367:379–384

    Google Scholar 

  • Guillery RW (1959) Afferent fibres to the dorsomedial thalamic nuclei in the cat. J Anat 93:403–419

    Google Scholar 

  • Haber SN, Nauta WJH (1983) Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry. Neuroscience 9:245–260

    Google Scholar 

  • Haber SN, Groenewegen HJ, Grove EA, Nauta WHJ (1985) Efferent connections of the ventral pallidum: evidence of a dual striato-pallidofugal pathway. Comp Neurol 235:322–325

    Google Scholar 

  • Heimer L, Wilson RD (1975) The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the pyriform cortex and the neocortex. In: Santini M (ed) Golgi centennial symposium. Raven, New York, pp 177–192

    Google Scholar 

  • Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89–125

    Google Scholar 

  • Hepler DJ, Olton DS, Wenk GL, Coyle JT (1985) Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments. J Neurosci 5:866–873

    Google Scholar 

  • Hubner CB, Koob GF (1990) The ventral pallidum plays a role in mediating cocaine and heroin self-administration in the rat. Brain Res 508:20–29

    Google Scholar 

  • Hunt SP, Pini A, Evan G (1987) Induction of c-Fos-like protein in the spinal cord neurons following sensory stimulation. Nature 328:632–634

    Google Scholar 

  • Imperato A, Scrocco MG, Bacchi S, Angelucci L (1990) NMDA receptors and in vivo dopamine release in the nucleus accumbens and caudatus. Eur J Pharmacol 187:555–556

    Google Scholar 

  • Ingham CA, Bolam JP, Smith AD (1988) GABA-immunoreactive synaptic boutons in the rat basal forebrain: comparison of neurons that project to the neocortex with pallidosubthalamic neurons. J Comp Neurol 273:263–282

    Google Scholar 

  • Jones BE, Cuello AC (1989) Afferents to the basal forebrain cholinergic cell area from pontomesencephalic catecholamine, serotonin and acetylcholine neurons. Neuroscience 31:37–61

    Google Scholar 

  • Krogsgaard-Larsen P, Honore T, Hansen JJ, Curtis DR, Lodge D (1980) New class of glutamate agonists structurally related to ibotenic acid. Nature 284:64–66

    Google Scholar 

  • Levey AI, Wainer BH, Rye DB, Mufson EJ, Mesulam M-M (1984) Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons. Neuroscience 13:341–353

    Google Scholar 

  • Markowska AL, Wenk GL, Olton DS (1990) Nucleus basalis magnocellularis and memory: differential effects of two neurotoxins. Behav Neural Biol 54:13–26

    Google Scholar 

  • Mesulam M-M, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1201

    Google Scholar 

  • Mogenson GJ, Neilson MA (1983) Evidence that an accumbens subpallidal GABAergic projection contributes to locomotor activity. Brain Res Bull 11:309–314

    Google Scholar 

  • Mogenson G, Neilson M (1984) Pharmacological evidence to suggest that the nucleus accumbens and subpallidal region contribute to exploratory locomotion. Behav Neural Biol 43:52–60

    Google Scholar 

  • Moghaddam B, Gruen RJ, Roth RH, Bunney BS, Adams RN (1990) Effect of l-glutamate on the release of striatal dopamine: in vivo dialysis and electrochemical studies. Brain Res 518:55–60

    Google Scholar 

  • Morgan JI, Curran T (1986) Role of ion flux in the control of c-fos expression. Nature 322:552–555

    Google Scholar 

  • Morgan JI, Curran T (1989) Stimulus-transcription coupling in neurons: role of cellular immediate early genes. Trends Neurosci 12:459–462

    Google Scholar 

  • Morgan JI, Cohen DR, Hempstead JL, Curran T (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237:192–196

    Google Scholar 

  • Nauta WJH, Domesick VB (1984) Afferent and efferent relationships of the basal ganglia. Ciba Found Symp 107:3–29

    Google Scholar 

  • Olton DS, Wenk GL (1987) Dementia: animal models of the cognitive impairments produced by degeneration of the basal forebrain cholinergic system. In: Meltzer H (ed) Psychopharmacology: the third generation of progress. Raven, New York, pp 941–953

    Google Scholar 

  • Page KJ, Everitt BJ, Robbins TW, Marston HM, Wilkinson LS (1991) Dissociable effects on spatial maze and passive avoidance acquisition and retention following AMPA- and ibotenic acidinduced excitotoxic lesions of the basal forebrain in rats: differential dependence on cholinergic neuronal loss. Neuroscience 43:457–472

    Google Scholar 

  • Page KJ, Saha A, Everitt BJ (1993) Differential activation and survival of basal forebrain neurons following infusions of excitatory amino acids: studies with the immediate early gene c-fos. Exp Brain Res

  • Parent A (1990) Extrinsic connections of the basal ganglia. Trends Neurosci 13:254–258

    Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic, Sydney

    Google Scholar 

  • Petralia RS, Wenthold RJ (1992) Light and electron microscopic immunocytochemical localisation of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318:329–354

    Google Scholar 

  • Robbins TW, Everitt BJ, Marston H, Wilkinson J, Jones GH, Page KJ (1989a) Comparative effects of ibotenic acid and quisqualic acid-induced lesions of the substantia innominata on attentional function in the rat: further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes. Behav Brain Res 35:221–240

    Google Scholar 

  • Robbins TW, Everitt BJ, Ryan CN, Marston HM, Jones GH, Page KJ (1989b) Comparative effects of quisqualic and ibotenic acidinduced lesions of the substantia innominata and globus pallidus on the acquisition of a conditional visual discrimination: differential effects on cholinergic mechanisms. Neuroscience 28:337–352

    Google Scholar 

  • Robertson GS, Fibiger HC (1992) Neuroleptics increase c-fos expression in the forebrain: contrasting effects of haloperidol and clozapine. Neuroscience 46:315–328

    Article  CAS  PubMed  Google Scholar 

  • Robertson HA, Peterson MR, Murphy K, Robertson GS (1989) D1-dopamine receptor agonists selectively activate striatal c-fos independent of rotational behaviour. Brain Res 503:346–349

    Google Scholar 

  • Robertson GS, Pfaus JG, Atkinson LJ, Matsumura H, Phillips AG, Fibiger HC (1991a) Sexual behaviour increases c-fos expression in the forebrain of the male rat. Brain Res 564:352–357

    Google Scholar 

  • Robertson HA, Paul ML, Moratalla R, Graybiel AM (1991b) Expression of the immediate early gene c-fos in basal ganglia: induction by dopaminergic drugs. Can J Neurol Sci 18:380–383

    Google Scholar 

  • Rye DB, Wainer BH, Mesulam M-M, Mufson EJ, Saper CB (1984) Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13:627–643

    Google Scholar 

  • Sagar SM, Sharp FR, Curran T (1988) Expression of C-Fos protein in brain: metabolic mapping at the cellular level. Science 240:1328–1330

    Google Scholar 

  • Saper CB (1987) Diffuse cortical projection systems: anatomical organization and role in cortical function. In: Mountcastle VB, Plum F, Geiger SR (eds) Handbook of physiology, vol 1. The nervous system, part 5. American Physiological Society, Bethesda, Maryland, pp 169–210

    Google Scholar 

  • Sarter M, Schneider HH (1988) High density of benzodiazepine binding sites in the substantia innominata of the rat. Pharmacol Biochem Behav 30:679–682

    Google Scholar 

  • Sarter M, Schneider HH, Stephens DN (1988) Treatment strategies for senile dementia: antagonist β-carbolines. Trends Neurosci 11:13–17

    Google Scholar 

  • Semba K, Rainer PB, McGeer EC, Fibiger HC (1988) Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry and electrophysiology in the rat. J Comp Neurol 267:433–453

    Google Scholar 

  • Smith AD, Bolam JP (1990) The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13:259–265

    Google Scholar 

  • Walaas I, Fonnum F (1979) The distribution and origin of glutamate decarboxylase and choline acetyltransferase in ventral pallidum and other basal forebrain regions. Brain Res 177:325–336

    Google Scholar 

  • Watkins JC, Krogsgaard-Larsen P, Honoré T (1990) Structureactivity relationships in the development of excitatory amino acid receptor agonists and competitive antagonists. Trends Pharmacol Sci 11:25–33

    Google Scholar 

  • Wenk GL, Olton DS (1987) Basal forebrain cholinergic neurons and Alzheimer's disease. In: Coyle JT (ed) Animal models of dementia: a synaptic neurochemical perspective. Liss, New York, pp 81–102

    Google Scholar 

  • Wenthold RJ, Yokotani N, Doi K, Keiji W (1992) Immunocytochemical characterisation of the non-NMDA glutamate receptor using subunit-specific antibodies. J Biol Chem 267:501–507

    Google Scholar 

  • Whishaw IQ, O'Connor WT, Dunnett SB (1985) Disruption of central cholinergic systems in the rat by basal forebrain lesions or atropine: effects on feeding, sensorimotor behaviour, locomotor activity and spatial navigation. Behav Brain Res 17:103–115

    Google Scholar 

  • Wood PL (1986) Pharmacological evaluation of GABAergic and glutamatergic inputs to the nucleus basalis-cortical and the septal-hippocampal cholinergic projections. Can J Physiol Pharmacol 64:325–328

    Google Scholar 

  • Young WS, Alheid GF, Heimer L (1984) The ventral pallidum projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence. J Neurosci 4:1626–1638

    Google Scholar 

  • Zaborszky L (1989) Afferent connections of the forebrain cholinergic projection neurons, with special reference to monoaminergic and peptidergic fibers. In: Frotscher M, Misgeld U (eds) Birkhauser, Basel, Central cholinergic synaptic transmission, pp 12–32

  • Zaborszky L, Cullinan WE (1989) Hypothalamic axons terminate on forebrain cholinergic neurons: an ultrastructural double labelling study using PHA-L tracing and ChAT immunocytochemistry. Brain Res 479:177–184

    Google Scholar 

  • Zaborszky L, Leranth C, Heimer L (1984) Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci Lett 52:219–225

    Google Scholar 

  • Zaborszky L, Heimer L, Eckenstein F, Leranth C (1986) GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabelling. J Comp Neurol 250:282–295

    Google Scholar 

  • Zahm DS, Heimer L (1988) Ventral striatopallidal parts of the basal ganglia in the rat: 1. Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreativity. J Comp Neurol 272:516–535

    Google Scholar 

  • Zahm DS, Heimer L (1990) Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol 302:437–446

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Anatomy, Cambridge University, Downing Street, CB2 3DY, Cambridge, UK

    Keith J. Page & Barry J. Everitt

Authors
  1. Keith J. Page
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barry J. Everitt
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Page, K.J., Everitt, B.J. Transsynaptic induction of c-fos in basal forebrain, diencephalic and midbrain neurons following AMPA-induced activation of the dorsal and ventral striatum. Exp Brain Res 93, 399–411 (1993). https://doi.org/10.1007/BF00229356

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229356

Key words

  • c-fos
  • FOS
  • Striatopallidal system
  • Subthalamic nucleus
  • Nucleus basalis magnocellularis
  • Rat