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Brain stem afferent connections of the amygdala in the rat with special references to a projection from the parabigeminal nucleus: a fluorescent retrograde tracing study

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Abstract

A recently revealed important function of the amygdala (Am) is that it acts as the brain’s “lighthouse”, which constantly monitors the environment for stimuli which signal a threat to the organism. The data from patients with extensive lesions of the striate cortex indicate that “unseen” fearful and fear-conditioned faces elicit increased Am responses. Thus, also extrageniculostriate pathways are involved. A multisynaptic pathway from the retina to the Am via the superior colliculus (SC) and the pulvinar was recently suggested. We here present data based on retrograde neuronal labeling following injection of the fluorescent tracer Fluoro-Gold in the rat Am that the parabigeminal nucleus (Pbg) emits a substantial, bilateral projection to the Am. This small cholinergic nucleus (Ch8 group) in the midbrain tegmentum is a subcortical relay visual center that is reciprocally connected with the SC. We suggest the existence of a second extrageniculo-striate multisynaptic connection to Am: retina–SC–Pbg–Am, that might be very effective since all tracts listed above are bilateral. In addition, we present hodological details on other brainstem afferent connections of the Am, some of which are only recently described, and some others that still remain equivocal. Following selective injections of Fluoro-Gold in the Am, retrogradely labeled neurons were observed in parasubthalamic nucleus, peripeduncular nucleus, periaqueductal gray, dopaminergic nuclear complex (substantia nigra pars lateralis and pars compacta, paranigral, parabrachial pigmented and interfascicular nuclei, rostral and caudal linear nuclei, retrorubral area), deep mesencephalic nucleus, serotoninergic structures (dorsal, median and pontine raphe nuclei), laterodorsal and pedunculopontine tegmental nuclei (Ch6 and Ch5 groups), parabrachial nuclear complex, locus coeruleus, nucleus incertus, ventrolateral pontine tegmentum (A5 group), dorsomedial medulla (nucleus of the solitary tract, A2 group), ventrolateral medulla (A1/C1 group), and pars caudalis of the spinal trigeminal nucleus. A bilateral labeling of the upper cervical spinal cord was also observed.

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Abbreviations

4V:

Fourth ventricle

5spi:

Spinal trigeminal nucleus, caudal part

7n:

Facial nerve

AP:

Area postrema

Aq:

Cerebral aqueduct

Am:

Amygdala

AmBl:

Amygdala, basolateral nucleus

AmBm:

Amygdala, basomedial nucleus

AmCe:

Amygdala, central nucleus

AmMe:

Amygdala, medial nucleus

Cc:

Central canal

CLi:

Caudal linear raphe nucleus

DpM:

Deep mesencephalic nucleus

FG:

Fluoro-Gold

HRP:

Horseradish peroxidase

If:

Interfascicular nucleus

LC:

Locus coeruleus

LCN:

Lateral cervical nucleus

LDTg:

Laterodorsal tegmental nucleus

DRD:

DRN, dorsal part

DRN:

Dorsal raphe nucleus

DRV:

DRN, ventral part

DRVL:

DRN, ventrolateral part

NI:

Midline nucleus incertus

me5:

Mesencephalic trigeminal tract

Me5:

Mesencephalic trigeminal nucleus

MRN:

Median raphe nucleus

PAG:

Periaqueductal gray

Pbg:

Parabigeminal nucleus

Pbp:

Nucleus parabrachialis pigmentosus

PbN:

Parabrachial nuclear complex

PbNel:

External lateral nucleus of the caudal PbN

PbNem:

External medial nucleus of the caudal PbN

PbNm:

Medial nucleus of the caudal PbN

PbNv:

Ventral lateral nucleus of the caudal PbN

ped:

Cerebral peduncle

PIL:

Posterior intralaminar thalamic nucleus

Pn:

Nucleus paranigralis

PP:

Peripeduncular nucleus

PPTg:

Pedunculopontine tegmental nucleus

PSTN:

Parasubthalamic nucleus

RLi:

Rostral linear raphe nucleus

RPn:

Raphe pontis nucleus

RR:

Retrorubral area (group A8)

scp:

Superior cerebellar peduncle

SN:

Substantia nigra

SNc:

SN pars compacta

SNl:

SN pars lateralis

SNr:

SN pars reticulata

SO:

Superior olive

Sol:

Nucleus of the solitary tract

STN:

Subthalamic nucleus

STrT:

Spinal trigeminal tract

VTA:

Ventral tegmental area (group A10)

References

  • Adolphs R, Tranel D (2000) Emotion, recognition, and the human amygdala. In: Aggleton JP (eds) The amygdala. A functional analysis, 2nd edn. Oxford University Press, Oxford, pp 587–630

    Google Scholar 

  • Adolphs R, Tranel D, Damasio H, Damasio A (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372:669–672

    PubMed  CAS  Google Scholar 

  • Adolphs R, Tranel D, Damasio H, Damasio AR (1995) Fear and the human amygdala. J Neurosci 15:5879–5891

    PubMed  CAS  Google Scholar 

  • Aggleton JP (ed) (1992) The amygdala: neurobiological aspects of emotion, memory and mental disfunction. Wiley-Liss, New York

  • Aggleton JP, Saunders RC (2000) The amygdala – what’s happened in the last decade? In: Aggleton JP (eds) The amygdala. A functional analysis, 2nd edn. Oxford University Press, Oxford, pp 1–30

    Google Scholar 

  • Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 190:347–368

    PubMed  CAS  Google Scholar 

  • Alheid GF, Heimer L, Switzer RC III (1990) Basal ganglia. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 483–582

    Google Scholar 

  • Amaral DG (2003) The amygdala, social behavior, and danger detection. Ann NY Acad Sci 1000:337–347

    PubMed  Google Scholar 

  • Amaral DG, Price JL, Pitkänen A, Carmichael ST (1992) Anatomical organization of the primate amygdaloid complex. In: Aggleton JP (eds) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, pp 1–66

    Google Scholar 

  • Anderson AK, Christoff K, Panitz D, De Rose E, Gabrieli JD (2003) Neural correlates of the automatic processing of threat facial signals. J Neurosci 23:5627–5633

    PubMed  CAS  Google Scholar 

  • Arsenault MY, Parent A, Seguela P, Descarries L (1988) Distribution and morphological characteristics of dopamine-immunoreactive neurons in the midbrain of the squirrel monkey (Saimiri sciureus). J Comp Neurol 267:489–506

    PubMed  CAS  Google Scholar 

  • Asan E (1995) The adrenergic innervation of the rat central amygdaloid nucleus: a light and electron microscopic immunocytochemical study using phenylethanolamine N-methyltransferase as a marker. Anat Embryol 192:471–481

    PubMed  CAS  Google Scholar 

  • Asan E (1997) Ultrastructural features of tyrosine-hydroxylase-immunoreactive afferents and their targets in the rat amygdala. Cell Tissue Res 288:449–469

    PubMed  CAS  Google Scholar 

  • Asan E (1998) The catecholaminergic innervation of the rat amygdala. Adv Anat Embryol Cell Biol 142:1–118

    PubMed  CAS  Google Scholar 

  • Asan E, Yilmazer-Hanke DM, Eliava M, Hantsch M, Lesch KP, Schmitt A (2005) The corticotropin-releasing factor (CRF)-system and monoaminergic afferents in the central amygdala: investigations in different mouse strains and comparison with the rat. Neuroscience 131:953–967

    PubMed  CAS  Google Scholar 

  • Aston-Jones G (2004) Locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic, San Diego, pp 259–294

    Google Scholar 

  • Aston-Jones G, Shipley MT, Grzanna R (1995) The locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos G (eds) The rat nervous system, 2nd edn. Academic Press, San Diego, pp 183–213

    Google Scholar 

  • Aston-Jones G, Rajkowski J, Kubiak P, Valentino RJ, Shipley MT (1996) Role of the locus coeruleus in emotional activation. Prog Brain Res 107:379–402

    PubMed  CAS  Google Scholar 

  • Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641–667

    PubMed  CAS  Google Scholar 

  • Baleydier C, Magnin M (1979) Afferent and efferent connections of the parabigeminal nucleus in cat revealed by retrograde axonal transport of horseradish peroxidase. Brain Res 161:187–198

    PubMed  CAS  Google Scholar 

  • Barnett EM, Evans GD, Sun N, Perlman S, Cassell MD (1995) Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1. J Neurosci 15:2972–2984

    PubMed  CAS  Google Scholar 

  • von Bechterew VM (1899) Die Leitungsbahnen in Gehirn und Rückenmark. Arthur Georgi, Leipzig, pp 132–240

    Google Scholar 

  • Beckstead RM, Domesick VB, Nauta WJH (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191–217

    PubMed  CAS  Google Scholar 

  • Ben-Ari Y (ed) (1981) The amygdaloid complex. Elsevier, Amsterdam

  • Benevento LA, Fallon JH (1975) The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J Comp Neurol 160:339–362

    PubMed  CAS  Google Scholar 

  • Berman AL (1968) The brain stem of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. The University of Wisconsin Press, Wisconsin

    Google Scholar 

  • Bernard JF, Besson JM (1990) The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 63:473–490

    PubMed  CAS  Google Scholar 

  • Bernard JF, Alden M, Besson JM (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329:201–229

    PubMed  CAS  Google Scholar 

  • Bernard JF Dallel R, Raboisson P, Villanueva L, Le Bars D (1995) Organization of the efferent projections from the spinal cervical enlargement to the parabrachial area and the periaqueductal gray: a PHA-L study in the rat. J Comp Neurol 353:480–505

    Google Scholar 

  • Bernard JF, Bester H, Besson JM (1996) Involvement of the spino-parabrachio-amygdaloid and hypothalamic pathways in the autonomic and affective emotional aspects of pain. Prog Brain Res 107:243–255

    PubMed  CAS  Google Scholar 

  • Bester H, Matsumoto N, Besson JM, Bernard JF (1997) Further evidence for the involvement of the spinoparabrachial pathway in nociceptive processes: a c-Fos study in the rat. J Comp Neurol 383:439–458

    PubMed  CAS  Google Scholar 

  • Bickford ME, Ramcharan E, Godwin DW, Erisir A, Gnadt J, Sherman SM (2000) Neurotransmitters contained in the subcortical extraretinal inputs to the monkey lateral geniculate nucleus. J Comp Neurol 424:701–717

    PubMed  CAS  Google Scholar 

  • Bina KG, Rusak B, Semba K (1993) Localization of cholinergic neurons in the forebrain and brainstem that project to the suprachiasmatic nucleus of the hypothalamus in rat. J Comp Neurol 335:295–307

    PubMed  CAS  Google Scholar 

  • Björklund A, Lindvall O (1975) Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res 83:531–537

    PubMed  Google Scholar 

  • Block CH, Estes ML (1990) The cytoarchitectural organization of the human parabrachial nuclear complex. Brain Res Bull 24:617–626

    PubMed  CAS  Google Scholar 

  • Bogerts B (1981) A brainstem atlas of catecholaminergic neurons in man, using melanin as a natural marker. J Comp Neurol 197:63–80

    PubMed  CAS  Google Scholar 

  • Braak H, Braak E (1986) Nuclear configuration and neuronal types of the nucleus niger in the brain of the human adult. Hum Neurobiol 5:71–82

    PubMed  CAS  Google Scholar 

  • Breitner HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman S, Rosen BR (1996) Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17:875–887

    Google Scholar 

  • Brockhaus H (1938) Zur normalen und pathologischen Anatomie des Mandelkerngebietes. J Psychol Neurol 49:1–136

    Google Scholar 

  • Brodal A (1947) The amygdaloid nucleus of the rat. J Comp Neurol 87:1–16

    CAS  PubMed  Google Scholar 

  • Burstein R, Potrebic S (1993) Retrograde labeling of neurons in the spinal cord that project directly to the amygdala or the orbital cortex in the rat. J Comp Neurol 335:469–485

    PubMed  CAS  Google Scholar 

  • Butcher LL, Oh JD, Woolf NJ, Edwards RH, Roghani A (1992) Organization of central cholinergic neurons revealed by combined in situ hybridization histochemistry and choline-O-acetyltransferase immunocytochemistry. Neurochem Int 21:429–445

    PubMed  CAS  Google Scholar 

  • Byrum CE, Guyenet PG (1987) Afferent and efferent connections of the A5 noradrenergic cell group in the rat. J Comp Neurol 261:529–542

    PubMed  CAS  Google Scholar 

  • Cahill L, Babinsky R, Markowitsch H, McGaugh JL (1995) The amygdala and emotional memory. Nature 377:295–296

    PubMed  CAS  Google Scholar 

  • Cameron AA, Khan IA, Westlund KN, Cliffer KD, Willis WD (1995) The efferent projections of the periaqeductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. I. Ascending projections. J Comp Neurol 351:568–584

    PubMed  CAS  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1992) Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143–179

    PubMed  CAS  Google Scholar 

  • Carlsen J (1989) New perspectives on the functional anatomical organization of the basolateral amygdala. Acta Neurol Scand Suppl 122:1–27

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Cechetto DF (1987) Central representation of visceral function. Fed Proc 46:17–23

    PubMed  CAS  Google Scholar 

  • Cechetto DF, Ciriello J, Calaresu FR (1983) Afferent connections to cardiovascular sites in the amygdala: a horseradish peroxidase study in the cat. J Auton Nerv Syst 8:97–110

    PubMed  CAS  Google Scholar 

  • Ciriello J, Schulz CG, Roder S (1994) Collateral axonal projections from ventrolateral medullary non-catecholaminergic neurons to central nucleus of the amygdala. Brain Res 663:346–351

    PubMed  CAS  Google Scholar 

  • Cliffer KD, Burstein R, Giesler GJ (1991) Distributions of spinothalamic, spinohypothalamic, and spinotelencephalic fibers revealed by anterograde transport of PHA-L in rats. J Neurosci 11:852–868

    PubMed  CAS  Google Scholar 

  • Cornwall J, Cooper JD, Phillipson OT (1990) Afferent and efferent connections of the laterodorsal tegmental nucleus: efferent and afferent connections. Brain Res Bull 25:271–284

    PubMed  CAS  Google Scholar 

  • Craig AD (1995) Distribution of brainstem projections from spinal lamina I neurons in the cat and monkey. J Comp Neurol 361:225–248

    PubMed  CAS  Google Scholar 

  • Cui H, Malpeli JG (2003) Activity in the parabigeminal nucleus during eye movements directed at moving and stationary targets. J Neurophysiol 89:3128–3142

    PubMed  Google Scholar 

  • Dahlström A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the mammalian nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol Scand Suppl 232:1–55

    Google Scholar 

  • Das P, Kemp AH, Liddell BJ, Brown KJ, Olivieri G, Peduto A, Gordon E, Williams LM (2005) Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems. Neuroimage 26:141–148

    PubMed  Google Scholar 

  • Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13–34

    PubMed  CAS  Google Scholar 

  • De Lima AD, Singer W (1987) The brainstem projection to the lateral geniculate nucleus in the cat: identification of cholinergic and monoaminergic elements. J Comp Neurol 259:92–121

    PubMed  Google Scholar 

  • Diamond IT, Fitzpatrick D, Conley M (1992) A projection from the parabigeminal nucleus to the pulvinar nucleus in Galago. J Comp Neurol 316:375–382

    PubMed  CAS  Google Scholar 

  • Dietrichs E (1985) Divergent axon collaterals to cerebellum and amygdala from neurons in the parabrachial nucleus, the nucleus locus coeruleus and some adjacent nuclei. A fluorescent double labeling study using rhodamine labeled latex microspheres and fast blue as retrograde tracers. Anat Embryol 172:375–382

    PubMed  CAS  Google Scholar 

  • Dobolyi A, Irwin S, Makara G, Usdin TB, Palkovits M (2005) Calcitonin gene-related peptide-containing pathways in the rat forebrain. J Comp Neurol 489:92–119

    PubMed  CAS  Google Scholar 

  • Eberhart JA, Morrell JI, Krieger MS, Pfaff DW (1985) An autoradiographic study of projections ascending from the midbrain central gray, and from the region lateral to it, in the rat. J Comp Neurol 241:285–310

    PubMed  CAS  Google Scholar 

  • Fallon JH, Loughlin SE (1982) Monoamine innervation of the forebrain: collateralization. Brain Res Bull 9:295–307

    PubMed  CAS  Google Scholar 

  • Fallon JH, Loughlin SE (1995) Substantia nigra. In: Paxinos G (eds) The rat nervous system, 2nd edn. Academic, San Diego, pp 215–237

    Google Scholar 

  • Fallon JH, Moore RY (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol 180:545–580

    PubMed  CAS  Google Scholar 

  • Fallon JH, Koziell DA, Moore RY (1978) Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol 180:509–532

    PubMed  CAS  Google Scholar 

  • Feig S, Harting JK (1994) Ultrastructural studies of the primate lateral geniculate nucleus: morphology and spatial relationships of axon terminals arising from the retina, visual cortex (area 17), superior colliculus, parabigeminal nucleus, and pretectum of Galago crassicaudatus. J Comp Neurol 343:17–34

    PubMed  CAS  Google Scholar 

  • Fitzpatrick D, Conley M, Luppino G, Matelli M, Diamond IT (1988) Cholinergic projections from the midbrain reticular formation and the parabigeminal nucleus to the lateral geniculate nucleus in the tree shrew. J Comp Neurol 272:43–67

    PubMed  CAS  Google Scholar 

  • Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319:229–259

    PubMed  CAS  Google Scholar 

  • Gallyas F, Hsu M, Buzsaki G (1993) Four modified silver methods for thick sections of formaldehyde-fixed mammalian central nervous tissue: ‘dark’ neurons, perikarya of all neurons, microglial cells and capillaries. J Neurosci Methods 50:159–164

    PubMed  CAS  Google Scholar 

  • Gauriau C, Bernard JF (2002) Pain pathways and parabrachial circuits in the rat. Exp Physiol 87:251–258

    PubMed  Google Scholar 

  • Gauriau C, Bernard JF (2004) A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: the forebrain. J Comp Neurol 468:24–56

    PubMed  Google Scholar 

  • Gerfen C (2004) Basal ganglia. In: Paxinos G (eds) The rat nervous system, 3rd edn. Elsevier Academic Press, San Diego, pp 458–509

    Google Scholar 

  • German DC, Manaye KF (1993) Midbrain dopaminergic neurons (nuclei A8, A9, and A10): three dimensional reconstruction in the rat. J Comp Neurol 331:297–309

    PubMed  CAS  Google Scholar 

  • Gorman JM, Kent JM, Sullivan GM, Coplan JD (2000) Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry 157:493–505

    PubMed  CAS  Google Scholar 

  • Goto M, Swanson LW (2004) Axonal projections from the parasubthalamic nucleus. J Comp Neurol 469:581–607

    PubMed  Google Scholar 

  • Goto M, Swanson LW, Canteras NS (2001) Connections of the nucleus incertus. J Comp Neurol 438:86–122

    PubMed  CAS  Google Scholar 

  • Graybiel AM (1978) A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers. Brain Res 145:365–374

    PubMed  CAS  Google Scholar 

  • Grieve KL, Acuna C, Cudeiro J (2000) The primate pulvinar nuclei: vision and action. Trends Neurosci 23:35–39

    PubMed  CAS  Google Scholar 

  • Hall E (1972) Some aspects of the structural organization of the amygdala. In: Eleftheriou BE (eds) The neurobiology of the amygdala. Plenum Press, New York, pp 95–121

    Google Scholar 

  • Hall WC, Fitzpatrick D, Klatt LL, Raczkowski D (1989) Cholinergic innervation of the superior colliculus in the cat. J Comp Neurol 287:495–514

    PubMed  CAS  Google Scholar 

  • Hallanger AE, Wainer BH (1988) Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J Comp Neurol 274:483–515

    PubMed  CAS  Google Scholar 

  • Halliday GM, Törk I (1986) Comparative anatomy of the ventromedial mesencephalic tegmentum in the rat, cat, monkey and human. J Comp Neurol 252:423–445

    PubMed  CAS  Google Scholar 

  • Halsell CB (1992) Organization of parabrachial nucleus efferents to the thalamus and amygdala in the golden hamster. J Comp Neurol 317:57–78

    PubMed  CAS  Google Scholar 

  • Harding A, Paxinos G, Paxinos G (2004) The serotonin and tachykinin systems. In: Paxinos G (eds) The rat nervous system, 2nd edn. Elsevier Academic Press, San Diego, pp 1203–1256

    Google Scholar 

  • Hariri AR, Tessitore A, Mattay VS, Fera F, Weinberger DR (2002) The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 17:317–323

    PubMed  Google Scholar 

  • Harting JK (1977) Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173:583–612

    PubMed  CAS  Google Scholar 

  • Harting JK, Hall WC, Diamond IT, Martin GF (1973) Anterograde degeneration study of the superior colliculus in tupaia glis: evidence for a subdivision between superficial and depp layers. J Comp Neurol 148:361–386

    PubMed  CAS  Google Scholar 

  • Harting JK, Van Lieshout DP, Hashikawa T, Weber JT (1991) The parabigeminogeniculate projection: Connectional studies in eight mammals. J Comp Neurol 305:559–581

    PubMed  CAS  Google Scholar 

  • Hashikawa T, Van Lishout D, Harting JK (1986) Projections from the parabigeminal nucleus to the dorsal lateral geniculate nucleus in the tree shrew Tupaia glis. J Comp Neurol 246:382–394

    PubMed  CAS  Google Scholar 

  • Hassler R (1937) Zur Normalanatomie der Substantia nigra. J Psychol Neurol 48:1–55

    Article  Google Scholar 

  • Heckers S, Mesulam MM (1994) Two types of cholinergic projections to the rat amygdala. Neuroscience 60:383–397

    Google Scholar 

  • Heimer L, de Olmos J, Alheid GF, Zaborszky L (1991) Perestroika in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res 87:109–165

    Article  PubMed  CAS  Google Scholar 

  • Heimer L, de Olmos JS, Alheid GF, Pearson J, Sakamoto N, Shinoda K, Marksteiner J, Switzer RC (1999) The human basal forebrain. Part II. In: Bloom FE, Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 15, The primate nervous system, part III. Elsevier, Amsterdam, pp 57–226

  • Henderson Z (1987) Cholinergic innervation of ferret visual system. Neuroscience 20:503–518

    PubMed  CAS  Google Scholar 

  • Herzog AG, Van Hoesen GW (1976) Temporal neocortical afferent connections to the amygdala in the rhesus monkey. Brain Res 115:57–69

    PubMed  CAS  Google Scholar 

  • Hökfelt T, Fuxe K, Goldstein M, Johansson O (1974) Immunohistochemical evidence for the existence of adrenaline neurons in the rat brain. Brain Res 66:235–251

    Google Scholar 

  • Hökfelt T, Johansson O, Goldstein M (1984) Central catecholamine neurons as revealed by immunohistochemistry with special reference to adrenaline neurons. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 2, part 1. Elsevier, Amsterdam, pp 157–276

  • Iidaka T, Omori M, Murata T, Kosaka H, Yonekura Y, Okada T, Sadato N (2001) Neural interaction of the amygdala with the prefrontal and temporal cortices in the processing of facial expressions as revealed by fMRI. J Cogn Neurosci 13:1035–1047

    PubMed  CAS  Google Scholar 

  • Imai H, Steindler DA, Kitai ST (1986) The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 243:363–380

    PubMed  CAS  Google Scholar 

  • Jeon CJ, Spencer RF, Mize RR (1993) Organization and synaptic connections of cholinergic fibers in the cat superior colliculus. J Comp Neurol 333:360–374

    PubMed  CAS  Google Scholar 

  • Jhamandas JH, Petrov T, Harris KH, Vu T, Krukoff TL (1996) Parabrachial nucleus projection to the amygdala in the rat: electrophysiological and anatomical observations. Brain Res Bull 39:115–126

    PubMed  CAS  Google Scholar 

  • Jiang ZD, King AJ, Moore DR (1996) Topographic organization of projection from the parabigeminal nucleus to the superior colliculus in the ferret revealed with fluorescent latex microspheres. Brain Res 743:217–232

    PubMed  CAS  Google Scholar 

  • Jones BE (2003) Arousal systems. Front Biosci 8:38–51

    Google Scholar 

  • Jones BE, Beaudet A (1987) Distribution of acetylcholine and catecholamine neurons in the cat brainstem: a choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J Comp Neurol 261:15–32

    PubMed  CAS  Google Scholar 

  • Jones EG, Burton H (1976) A projection from the medial pulvinar to the amygdala in primates. Brain Res 104:142–147

    PubMed  CAS  Google Scholar 

  • Jones BE, Moore RY (1977) Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study. Brain Res 127:125–153

    Google Scholar 

  • Jones EG, Burton H, Saper CB, Swanson LW (1976) Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J Comp Neurol 167:385–420

    PubMed  CAS  Google Scholar 

  • Kaada BR (1972) Stimulation and regional ablation of amygdaloid complex with reference to functional representations. In: Eleftheriou BE (ed) The neurobiology of the amygdala. Plenum Press, New York, pp 205–281

    Google Scholar 

  • Kaelber WW (1978) The relationship of the locus coeruleus to the amygdala in the cat. J Anat 127:469–473

    PubMed  CAS  Google Scholar 

  • Kaelber WW, Afifi AK (1977) Nigro-amygdaloid fiber connections in the cat. Am J Anat 148:129–135

    PubMed  CAS  Google Scholar 

  • Kalia M, Fuxe K, Goldstein M (1985a) Rat medulla oblongata. II. Dopaminergic, noradrenergic (A1 and A2) and adrenergic neurons, nerve fibers, and presumptive terminal processes. J Comp Neurol 233:308–332

    CAS  Google Scholar 

  • Kalia M, Fuxe K, Goldstein M (1985b) Rat medulla oblongata. III. Adrenergic (C1 and C2) neurons, nerve fibers, and presumptive terminal processes. J Comp Neurol 233:333–349

    CAS  Google Scholar 

  • Kapp BS, Markgraf CG, Schwaber JS, Bilyk-Spafford T (1989) The organization of dorsal medullary projections to the central amygdaloid nucleus and parabrachial nuclei in the rabbit. Neuroscience 30:717–732

    PubMed  CAS  Google Scholar 

  • Karimnamazi H, Travers JB (1998) Differential projections from gustatory responsive regions of the parabrachial nucleus to the medulla and forebrain. Brain Res 813:283–302

    PubMed  CAS  Google Scholar 

  • Kemppainen S, Pitkänen A (2000) Distribution of parvalbumin, calretinin, and calbindin-D(28k) immunoreactivity in the rat amygdaloid complex and colocalization with gamma-aminobutyric acid. J Comp Neurol 426:441–467

    PubMed  CAS  Google Scholar 

  • Klop EM, Mouton LJ, Hulsebosch R, Boers J, Holstege G (2005) In cat four times as many lamina I neurons project to the parabrachial nuclei and twice as many to the periaqueductal gray as to the thalamus. Neuroscience 134:189–197

    PubMed  CAS  Google Scholar 

  • Koikegami H (1963) Amygdala and other related limbic structures. Experimental studies on the anatomy and function. I. Anatomical researches with some neurophysiological observations. Acta Med Biol (Niigata) 10:161–277

    CAS  Google Scholar 

  • Kolesarova D, Petrovicky P (1987) Parabrachial nuclear complex in the rat (nuclei parabrachiales and nucleus Koelliker-Fuse). Detailed cytoarchitectonic division and connections compared. J Hirnforsch 28:517–527

    PubMed  CAS  Google Scholar 

  • Kordower JH, Bartus RT, Marciano FF, Gash DM (1989) Telencephalic cholinergic system of the New World monkey (Cebus apella): morphological and cytoarchitectonic assessment and analysis of the projection to the amygdala. J Comp Neurol 279:528–545

    PubMed  CAS  Google Scholar 

  • Krettek JE, Price JL (1978) A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol 178:255–280

    PubMed  CAS  Google Scholar 

  • Krukoff TL, Harris KH, Jhamandas JH (1993) Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res Bull 30:163–172

    PubMed  CAS  Google Scholar 

  • Künzle H (1997) Connections of the superior colliculus with the tegmentum and the cerebellum in the hedgehog tenrec. Neurosci Res 28:127–145

    PubMed  Google Scholar 

  • Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: projections to the basal ganglia as revealed by anterograde tract-tracing methods. J Comp Neurol 344:210–231

    PubMed  CAS  Google Scholar 

  • LeDoux JE (2000a) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184

    CAS  Google Scholar 

  • LeDoux JE (2000b) The amygdala and emotion: a view through fear. In: Aggleton JP (eds) The amygdala. A functional analysis, 2nd edn. Oxford University Press, Oxford, pp 289–310

    Google Scholar 

  • Lee PH, Schmidt M, Hall WC (2001) Excitatory and inhibitory circuitry in the superficial gray layer of the superior colliculus. J Neurosci 21:8145–8153

    PubMed  CAS  Google Scholar 

  • Liddell BJ, Brown KJ, Kemp AH, Barton MJ, Das P, Peduto A, Gordon E, Williams LM (2005) A direct brainstem-amygdala-cortical “alarm” system for subliminal signals of fear. Neuroimage 24:235–243

    PubMed  Google Scholar 

  • Linke R, De Lima AD, Schwegler H, Pape HC (1999) Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J Comp Neurol 403:158–170

    PubMed  CAS  Google Scholar 

  • Lolova I, Davidoff M (1990) Histo- and immunohistochemical changes in acetylcholinesterase and choline acetyltransferase activities in the amygdaloid complex in aged rats. Acta Histochem 89:173–182

    PubMed  CAS  Google Scholar 

  • Loughlin SE, Fallon JH (1983) Dopaminergic and non-dopaminergic projections to amygdala from substantia nigra and ventral tegmental area. Brain Res 262:334–338

    PubMed  CAS  Google Scholar 

  • Ma W, Peschanski M (1988) Spinal and trigeminal projections to the parabrachial nucleus in the rat: electron-microscopic evidence of a spino-ponto-amygdalian somatosensory pathway. Somatosens Res 5:247–257

    Article  PubMed  CAS  Google Scholar 

  • Manger PR, Fahringer HM, Pettigrew JD, Siegel JM (2002) The distribution and morphological characteristics of cholinergic cells in the brain of monotremes as revealed by ChAT immunohistochemistry. Brain Behav Evol 60:275–297

    PubMed  CAS  Google Scholar 

  • Maren S (2005) Building and burying fear memories in the brain. Neuroscientist 11:89–99

    PubMed  Google Scholar 

  • Mason ST, Fibiger HC (1979) Regional topography within noradrenergic locus coeruleus as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 187:703–724

    PubMed  CAS  Google Scholar 

  • McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332

    PubMed  CAS  Google Scholar 

  • McGaugh JL, Cahill L, Roozendaal B (1996) Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci USA 93:13508–13514

    PubMed  CAS  Google Scholar 

  • Mehler WR (1980) Subcortical afferent connections of the amygdala in the monkey. J Comp Neurol 190:733–762

    PubMed  CAS  Google Scholar 

  • Meller ST, Dennis BJ (1991) Efferent projections of the periaqueductal gray in the rabbit. Neuroscience 40:191–216

    PubMed  CAS  Google Scholar 

  • Menetrey D, De Pomery J (1991) Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur J Neurosci 3:249–259

    PubMed  Google Scholar 

  • Mesulam MM, 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

    PubMed  CAS  Google Scholar 

  • Mesulam MM, Geula C, Bothwell MA, Hersh LB (1989) Human reticular formation: cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J Comp Neurol 283:611–633

    PubMed  CAS  Google Scholar 

  • Moore RY, Card JP (1984) Noradrenaline-containing neuron systems. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy. vol 2, Classical transmitters in the CNS, part II. Elsevier, Amsterdam, pp 123–156

  • Moore RY, Halaris AE, Jones BE (1978) Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol 180:417–438

    PubMed  CAS  Google Scholar 

  • Moore RY, Whone AL, McGowan S, Brooks DJ (2003) Monoamine neuron innervation of the normal human brain: an 18F-DOPA PET study. Brain Res 982:137–145

    PubMed  CAS  Google Scholar 

  • Morris JS, Ohman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci USA 96:1680–1685

    PubMed  CAS  Google Scholar 

  • Morris JS, DeGelder B, Weiskrantz L, Dolan RJ (2001) Differential extrageniculostriate and amygdala responces to presentation of emotional faces in a cortically blind field. Brain 124:1241–1252

    PubMed  CAS  Google Scholar 

  • Mufson EJ, Martin TL, Mash DC, Wainer BH, Mesulam MM (1986) Cholinergic projections from the parabigeminal nucleus (Ch8) to the superior colliculus in the mouse: a combined analysis of horseradish peroxidase transport and choline acetyltransferase immunohistochemistry. Brain Res 370:144–148

    PubMed  CAS  Google Scholar 

  • Neugebauer V, Li W, Bird GC, Han JS (2004) The amygdala and persistent pain. Neuroscientist 10:221–234

    PubMed  Google Scholar 

  • Newman HM, Stevens RT, Apkarian AV (1996) Direct spinal projections to limbic and striatal areas: anterograde transport studies from the upper cervical spinal cord and the cervical enlargement in squirrel monkey and rat. J Comp Neurol 365:640–658

    PubMed  CAS  Google Scholar 

  • Nomura S, Mizuno N, Itoh K, Matsuda K, Sugimoto T, Nakamura Y (1979) Localization of parabrachial neurons projecting to the thalamus or the amygdala in the cat using horseradish peroxidase. Exp Neurol 64:375–385

    PubMed  CAS  Google Scholar 

  • van Noort J (1969) The structure and connections of the inferior colliculus. Thesis. Van Gorcum, Assen

  • de Olmos JS (1990) Amygdala. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 583–710

    Google Scholar 

  • de Olmos JS, Beltramino CA, Alheid G (2004) Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In: Paxinos G (ed) The rat nervous system, 3rd edn. Academic, San Diego, pp 509–603

    Google Scholar 

  • Olszewski J, Baxter D (1954) Cytoarchitecture of the human brain stem. Karger, Basel

    Google Scholar 

  • Olucha-Bordonau FE, Teruel V, Barcia-Gonzalez J, Ruz-Torner A, Valverde-Navarro AA, Martinez-Soriano F (2003) Cytoarchitecture and efferent projections of the nucleus incertus of the rat. J Comp Neurol 464:62–97

    PubMed  Google Scholar 

  • Ottersen OP (1981) Afferent connections to the amygdaloid complex of the rat with some observations in the cat. III. Afferents from the lower brain stem. J Comp Neurol 202:335–356

    PubMed  CAS  Google Scholar 

  • Oya H, Kawasaki H, Howard MA 3rd, Adolphs R (2002) Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 22:9502–9512

    PubMed  CAS  Google Scholar 

  • Parent A (1996) Carpenter’s human neuroanatomy, 9th edn. Williams and Wilkins, Baltimore

    Google Scholar 

  • Paxinos G, Huang XF (1995) Atlas of the human brainstem. Academic , San Diego

    Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic, San Diego

    Google Scholar 

  • Paxinos G, Törk I, Halliday G, Mehler WR (1990) Human homologs to brainstem nuclei identified in other animals as revealed by acetylcholinesterase activity. In: Paxinos G (eds) The human nervous system. Academic, San Diego, pp 149–202

    Google Scholar 

  • Paxinos G, Kus L, Ashwell KWS, Watson C (1999) Chemoarchitectonic atlas of the rat forebrain. Academic, San Diego

    Google Scholar 

  • Pearson J, Halliday G, Sakamoto N, Michel JP (1990) Catecholaminergic neurons. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 1023–1049

    Google Scholar 

  • Petrov T, Krukoff TL, Jhamandas JH (1993) Branching projections of catecholaminergic brainstem neurons to the paraventricular hypothalamic nucleus and the central nucleus of the amygdala in the rat. Brain Res 609:81–92

    PubMed  CAS  Google Scholar 

  • Petrov T, Krukoff TL, Jhamandas JH (1994) Chemically defined collateral projections from the pons to the central nucleus of the amygdale and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 277:289–295

    PubMed  CAS  Google Scholar 

  • Petrovich GD, Gallagher M (2003) Amygdala subsystems and control of feeding behavior by learned cues. Ann NY Acad Sci 985:251–262

    Article  PubMed  Google Scholar 

  • Pickel VM, Segal M, Bloom FE (1974) A radioautographic study of the efferent pathways of the nucleus locus coeruleus. J Comp Neurol 155:15–42

    PubMed  CAS  Google Scholar 

  • Pitkänen A (2000) Connectivity of the rat amygdaloid complex. In: Aggleton JP (ed) The amygdala: a functional analysis. Oxford University Press, Oxford, pp 31–115

    Google Scholar 

  • Poirier LJ, Giguere M, Marchand R (1983) Comparative morphology of the substantia nigra and of the ventral tegmental area in the monkey, cat and rat. Brain Res Bull 11:371–397

    PubMed  CAS  Google Scholar 

  • Pretorius JK, Phelan KD, Mehler WR (1979) Afferent connections of the amygdala in rat. Anat Rec 187:657

    Google Scholar 

  • Price DD (2002) Central neural mechanisms that interrelate sensory and affective dimensions of pain. Mol Interv 2:392–403

    PubMed  Google Scholar 

  • Price JL (2003) Comparative aspects of amygdala connectivity. Ann NY Acad Sci 985:50–58

    Article  PubMed  Google Scholar 

  • Price JL, Russchen FT, Amaral DG (1987) The limbic region: II: The amygdaloid complex. In: Björklund A, Hökfelt T, Swanson LW (eds) Handbook of chemical neuroanatomy, vol 5, Integrated systems of the CNS, part I. Elsevier, Amsterdam, pp 289–381

    Google Scholar 

  • Pritchard TC, Hamilton RB, Norgren R (2000) Projections of the parabrachial nucleus in the old world monkey. Exp Neurol 165:101–117

    PubMed  CAS  Google Scholar 

  • Rasia-Filho AA, Londero RG, Achaval M (2000) Functional activities of the amygdala: an overview. J Psychiatry Neurosci 25:14–23

    PubMed  CAS  Google Scholar 

  • Reichling DB, Basbaum AI (1991) Collateralization of periaqueductal gray neurons to forebrain or diencephalon and to the medullary nucleus raphe magnus in the rat. Neuroscience 42:183–200

    PubMed  CAS  Google Scholar 

  • Ricardo JA, Koh ET (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res 153:1–26

    PubMed  CAS  Google Scholar 

  • Riche D, De Pommery J, Menetrey D (1990) Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J Comp Neurol 293:399–424

    PubMed  CAS  Google Scholar 

  • Rizvi TA, Ennis M, Behbehani MM, Shipley MT (1991) Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303:121–131

    PubMed  CAS  Google Scholar 

  • Roder S, Ciriello J (1993) Innervation of the amygdaloid complex by catecholaminergic cell groups of the ventrolateral medulla. J Comp Neurol 332:105–122

    PubMed  CAS  Google Scholar 

  • Roder S, Ciriello J (1994) Collateral axonal projections to limbic structures from ventrolateral medullary A1 noradrenergic neurons. Brain Res 638:182–188

    PubMed  CAS  Google Scholar 

  • Roldan M, Reinoso-Suarez F, Tortelly A (1983) Parabigeminal projections to the superior colliculus in the cat. Brain Res 280:1–13

    PubMed  CAS  Google Scholar 

  • Rolls E (2000) Neurophysiology and functions of the primate amygdala, and the neural basis of emotion. In: Aggleton JP (eds) The amygdala. A functional analysis. 2nd edn. Oxford University Press, Oxford, pp 447–478

    Google Scholar 

  • Russchen FT (1982) Amygdalopetal projections in the cat. II. Subcortical afferent connections. A study with retrograde tracing techniques. J Comp Neurol 207:157–176

    PubMed  CAS  Google Scholar 

  • Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat. Cytoarchitecture, cytochemistry and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483–528

    PubMed  CAS  Google Scholar 

  • Sadikot AF, Parent A (1990) The monoaminergic innervation of the amygdala in the squirrel monkey: an immunohistochemical study. Neuroscience 36:431–447

    PubMed  CAS  Google Scholar 

  • Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834

    PubMed  CAS  Google Scholar 

  • Saper CB (1990) Cholinergic systems. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 1095–1113

    Google Scholar 

  • Saper CB (2004) Central autonomic system. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic Press, San Diego, pp 761–794

    Google Scholar 

  • Saper CB, Loewy AD (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res 197:291–317

    PubMed  CAS  Google Scholar 

  • Saper CB, Loewy AD (1982) Projections of the pedunculopontine tegmental nucleus in the rat: evidence for additional extrapyramidal circuitry. Brain Res 252:367–372

    PubMed  CAS  Google Scholar 

  • Saper CB, Petito CK (1982) Correspondence of melanin-pigmented neurons in human brain with A1–A14 catecholamine cell groups. Brain 105:87–101

    PubMed  CAS  Google Scholar 

  • Sarhan M, Freund-Mercier MJ, Veinante P (2005) Branching patterns of parabrachial neurons projecting to the central extended amygdala: single axonal reconstructions. J Comp Neurol 491:418–442

    PubMed  Google Scholar 

  • Satoh K, Fibiger HC (1986) Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol 253:277–302

    PubMed  CAS  Google Scholar 

  • Schumann CM, Amaral DG (2005) Stereological estimation of the number of neurons in the human amygdaloid complex. J Comp Neurol 491:320–329

    PubMed  Google Scholar 

  • Schwaber JS, Sternini C, Brecha NC, Rogers WT, Card JP (1988) Neurons containing calcitonin gene-related peptide in the parabrachial nucleus project to the central nucleus of the amygdale. J Comp Neurol 270:416–426

    PubMed  CAS  Google Scholar 

  • Selden NR, Gitelman DR, Salamon-Murayama N, Parrish TB, Mesulam MM (1998) Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain. Brain 121:2249–2257

    PubMed  Google Scholar 

  • Shammah-Lagnado SJ, Alheid GF, Heimer L (1999) Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat. Neuroscience 94:1097–1123

    PubMed  CAS  Google Scholar 

  • Sherk H (1979) A comparison of visual-response properties in cat’s parabigeminal nucleus and superior colliculus. J Neurophysiol 42:1640–1655

    PubMed  CAS  Google Scholar 

  • Shi C, Davis M (2001) Visual pathways involved in fear conditioning measured with fear-potentiated stratle: behavioral and anatomic studies. J Neurosci 21:9844–9855

    PubMed  CAS  Google Scholar 

  • Steinbusch HWM, Nieuwenhuys R (1983) The raphe nuclei of the rat brainstem: a cytoarchitectonic and imunohistochemical study. In: Emson PC (ed) Chemical neuroanatomy. Raven Press, New York, pp 131–207

    Google Scholar 

  • Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321–353

    PubMed  CAS  Google Scholar 

  • Swanson LW (1992) Brain maps: structure of the rat brain. Elsevier, Amsterdam

    Google Scholar 

  • Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331

    PubMed  CAS  Google Scholar 

  • Tabbert K, Stark R, Kirsch P, Vaitl D (2005) Hemodynamic responses of the amygdala, the orbitofrontal cortex and the visual cortex during a fear conditioning paradigm. Int J Psychophysiol 57:15–23

    PubMed  Google Scholar 

  • Todd AJ, McGill MM, Shehab SA (2000) Neurokinin 1 receptor expression by neurons in laminae I, III and IV of the rat spinal dorsal horn that project to the brainstem. Eur J Neurosci 12:689–700

    PubMed  CAS  Google Scholar 

  • Tokunaga A, Otani K (1978) Neuronal organization of the corpus parabigeminum in the rat. Exp Neurol 58:361–375

    PubMed  CAS  Google Scholar 

  • Usunoff KG (1990) Cytoarchitectural, ultrastructural and histochemical characterization of substantia nigra. DSc Thesis, Vols I-VI. Medical Academy, Sofia

  • Usunoff KG, Kharazia VN, Valtschanoff JG, Schmidt HHHW, Weinberg RJ (1999) Nitric oxide synthase-containing projections to the ventrobasal thalamus in the rat. Anat Embryol 200:265–281

    PubMed  CAS  Google Scholar 

  • Usunoff KG, Itzev DE, Ovtscharoff WA, Marani E (2002) Neuromelanin in the human brain: a review and atlas of pigmented cells in the substantia nigra. Arch Physiol Biochem 110:257–369

    Article  PubMed  CAS  Google Scholar 

  • Usunoff KG, Itzev DE, Lolov SR, Wree A (2003) Pedunculopontine tegmental nucleus. Part I: cytoarchitecture, transmitters, development and connections. Biomed Rev 14:95–120

    Google Scholar 

  • Usunoff KG, Popratiloff A, Schmitt O, Wree A (2006a) Functional neuroanatomy of pain. Adv Anat Embryol Cell Biol 184:1–115

    CAS  Google Scholar 

  • Usunoff KG, Itzev DE, Schmitt O, Wree A (2006b) Brainstem projections to the amygdala. Ann Anat 188 (Suppl) (in press)

  • Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643–648

    PubMed  CAS  Google Scholar 

  • Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555–582

    PubMed  CAS  Google Scholar 

  • Vincent SR (2000) The ascending reticular activating system – from aminergic neurons to nitric oxide. J Chem Neuroanat 18:23–30

    PubMed  CAS  Google Scholar 

  • Vincent SR, Reiner PB (1987) The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371–415

    PubMed  CAS  Google Scholar 

  • Volz HP, Rehbein G, Triepel J, Knuepfer MM, Stumpf H, Stock G (1990) Afferent connections of the nucleus centralis amygdalae. A horseradish peroxidase study and literature survey. Anat Embryol 181:177–194

    PubMed  CAS  Google Scholar 

  • Voshart K, van der Kooy D (1981) The organization of the efferent projections of the parabrachial nucleus of the forebrain in the rat: a retrograde fluorescent double-labeling study. Brain Res 212:271–286

    PubMed  CAS  Google Scholar 

  • Wang PY (1995) Outlines and atlas of learning rat brain. Northwest University of Xian. Xian, China

  • Wang SR (2003) The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Res Rev 41:13–25

    PubMed  CAS  Google Scholar 

  • Wang CC, Willis WD, Westlund KN (1999) Ascending projections from the area around the spinal cord central canal: a Phaseolus vulgaris leucoagglutinin study in rats. J Comp Neurol 415:341–367

    PubMed  CAS  Google Scholar 

  • Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418

    PubMed  CAS  Google Scholar 

  • Williams MA, Morris AP, McGlone F, Abbott DF, Mattingley JB (2004) Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J Neurosci 24:2898–2904

    PubMed  CAS  Google Scholar 

  • Williams LM, Barton MJ, Kemp AH, Liddell BJ, Peduto A, Gordon E, Bryant RA (2005) Distinct amygdala-autonomic arousal profiles in response to fear signals in healthy males and females. Neuroimage 28:618–626

    PubMed  Google Scholar 

  • Wilson JR, Hendrickson AE, Sherk H, Tigges J (1995) Sources of subcortical afferents to the macaque’s dorsal lateral geniculate nucleus. Anat Rec 242:566–574

    PubMed  CAS  Google Scholar 

  • Woolf NJ, Butcher LL (1986) Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603–637

    PubMed  CAS  Google Scholar 

  • Woolf NJ, Harrison JB, Buchwald JS (1990) Cholinergic neurons of the feline pontomesencephalon. II. Ascending anatomical projections. Brain Res 520:55–72

    PubMed  CAS  Google Scholar 

  • Yamano M, Hillyard CJ, Girgis S, MacIntyre I, Emson PC, Tohyama M (1988a) Presence of a substance P-like immunoreactive neurone system from the parabrachial area to the central amygdaloid nucleus of the rat with reference to coexistence with calcitonin gene-related peptide. Brain Res 451:179–188

    CAS  Google Scholar 

  • Yamano M, Hillyard CJ, Girgis S, Emson PC, MacIntyre I, Tohyama M (1988b) Projections of neurotensin-like immunoreactive neurons from the lateral parabrachial area to the central amygdaloid nucleus of the rat with reference to the coexistence with calcitonin gene-related peptide. Exp Brain Res 71:603–610

    CAS  Google Scholar 

  • Yamashiro T, Satoh K, Nakagawa K, Moriyama H, Yagi T, Takada K (1998) Expression of Fos in the rat forebrain following experimental tooth movement. J Dent Res 77:1920–1925

    Article  PubMed  CAS  Google Scholar 

  • Yaniv D, Desmedt A, Jaffard R, Richter-Levin G (2004) The amygdala and appraisal processes: stimulus and response complexity as an organizing factor. Brain Res Rev 44:179–186

    PubMed  Google Scholar 

  • Yasui Y, Saper CB, Cechetto DF (1991) Calcitonin gene-related peptide (CGRP) immunoreactive projections from the thalamus to the striatum and amygdala in the rat. J Comp Neurol 308:293–310

    PubMed  CAS  Google Scholar 

  • Yoshimura N, Kawamura M, Masaoka Y, Homma I (2005) The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions. Neuroscience 131:523–534

    PubMed  CAS  Google Scholar 

  • Young AW, Aggleton JP, Hellawell DJ, Johnson M, Broks P, Hanley JR (1995) Face processing impairments after amygdalotomy. Brain 118:15–24

    PubMed  Google Scholar 

  • Zald DH (2003) The human amygdala and the emotional evaluation of sensory stimuli. Brain Res Rev 41:88–123

    PubMed  Google Scholar 

  • Zardetto-Smith AM, Gray TS (1995) Catecholamine and NPY efferents from the ventrolateral medulla to the amygdala in the rat. Brain Res Bull 38:253–260

    PubMed  CAS  Google Scholar 

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Acknowledgements

The expert technical assistance of Mrs. Barbara Kuhnke (Rostock), Mrs. Ekaterina A. Zlatanova, Mrs. Snejina S. Ilieva (Sofia) and Mrs. Elena I. Ivanova (Sofia) is gratefully acknowledged. Grant sponsor: National Science Fund of Bulgaria (No L1012/2001).

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  1. Department of Anatomy and Histology, Faculty of Medicine, Medical University, Sofia, 1431, Bulgaria

    K. G. Usunoff

  2. Institute of Physiology, Bulgarian Academy of Sciences, Sofia, 1113, Bulgaria

    K. G. Usunoff & D. E. Itzev

  3. Institute of Anatomy, Faculty of Medicine, University of Rostock, P.O. Box 10 08 88, 18055, Rostock, Germany

    K. G. Usunoff, O. Schmitt & A. Wree

  4. Department of Neurology, Faculty of Medicine, University of Rostock, P.O. Box 10 08 88, 18055, Rostock, Germany

    A. Rolfs

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Usunoff, K.G., Itzev, D.E., Rolfs, A. et al. Brain stem afferent connections of the amygdala in the rat with special references to a projection from the parabigeminal nucleus: a fluorescent retrograde tracing study. Anat Embryol 211, 475–496 (2006). https://doi.org/10.1007/s00429-006-0099-8

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  • DOI: https://doi.org/10.1007/s00429-006-0099-8

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