Anatomic heterogeneity of the rat amygdaloid complex

• Autorzy: Pitkanen A , Jolkkonen E. , Kemppainen S.
• Języki publikacji: EN

Abstrakty

EN

The amygdala is a nuclear complex composed of 13 nuclei and cortical areas and their subdivisions. Tract-tracing studies performed over the past 20 years demonstrate that each nucleus is uniquely connected with other brain areas. Consistent with anatomic heterogeneity, the functions of the amygdala vary from attention to memory to formation of emotional responses to sensory stimuli. Here, we briefly review the principles of amygdaloid neuronal wiring that underlie the computations necessary to perform such complex behavioural functions.

Słowa kluczowe

EN

epilepsy; emotion; amygdala; cortical area; brain area; rat

• Wydawca: -
• Czasopismo: Folia Morphologica
• Rocznik: 2000
• Tom: 59
• Numer: 1
• Opis fizyczny: p.1-23,fig.

Twórcy

autor

Pitkanen A

• University of Kuopio, POBox 1627, FIN-70 211 Kuopio, Finland

autor

Jolkkonen E.

autor

Kemppainen S.

Bibliografia

• 1. 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.
• 2. Adolphs R, Tranel D, Damasio AR (1998) The human amygdala in social judgement. Nature, 393: 470–474.
• 3. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31: 571–591.
• 4. Amaral DG, Price JL, Pitkänen A, Carmichael ST (1992) Anatomical organization of the primate amygdaloid complex. In: Aggleton JP (ed.). The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction. Wiley-Liss Publishers, New York, pp. 1–66.
• 5. Bacon SJ, Headlam AJN, Gabbott PLA, Smith AD (1996) Amygdala input to medial prefrontal cortex (mPFC) in the rat: A light and electron microscope study. Brain Res, 720: 211–219.
• 6. Bauman M, Kemper TL (1985) Histoanatomic observations of the brain in early infantile autism. Neurology, 35: 866–874.
• 7. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR (1995) Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science, 269: 1115–1118.
• 8. Beckstead RM (1978) Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell-labeling with horseradish peroxidase. Brain Res, 152: 249–264.
• 9. Behan M, Haberly LB (1999) Intrinsic and efferent connections of the endopiriform nucleus in rat. J Comp Neurol, 408: 532–548.
• 10. Berendse HW, Galis-de-Graaf Y, Groenewegen HJ (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol, 316: 314–347.
• 11. Bernard JF, Peschanski M, Besson JM (1989) A possible spino (trigemino)-ponto-amygdaloid pathway for pain. Neurosci Lett, 100: 83–88.
• 12. Bernard J-F, Alden M, Besson J-M (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.
• 13. Bianchi R, Corsetti G, Rodella L, Tredici G, Gioia M (1998) Supraspinal connections and termination patterns of the parabrachial complex determined by the biocytin anterograde tract-tracing in the rat. J Anat, 193: 417–430.
• 14. Bonda E, Petrides M, Ostry D, Evans A (1996) Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J Neurosci, 16: 3737–3744.
• 15. Braak H, Braak E, Yilmazer D (1994) Amygdala pathology in Parkinson’s disease. Acta Neuropathol (Berl.), 88: 493–500.
• 16. Brindley-Reed M, Mascani F, McDonald AJ (1995) Synaptology of prefrontal cortical projections to the basolateral amygdala: an electron microscopic study in the rat. Neurosci Lett, 202: 45–48.
• 17. Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993) The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol, 338: 255–278.
• 18. Caffe AR, van Leeuwen FW, Luiten PG (1987) Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus. J Comp Neurol, 261: 237–252.
• 19. Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) The amygdala and emotional memory. Nature, 377: 295–296.
• 20. Cahill L, McGaugh JL (1998) Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci, 21: 294–299.
• 21. Calderazzo L, Cavalheiro EA, Macchi G, Molinari M, Bentivoglio M (1996) Branched connections to the septum and to the entorhinal cortex from the hippocampus, amygdala and diencephalon in the rat. Brain Res Bull, 40: 245–251.
• 22. Canteras NS, Simerly RB, Swanson LW (1992a) Connections of the posterior nucleus of the amygdala. J Comp Neurol, 324: 143–179.
• 23. Canteras NS, Simerly RB, Swanson LW (1992b) Projections of the ventral premammillary nucleus. J Comp Neurol, 324: 195–212.
• 24. Canteras NS, Simerly RB, Swanson LW (1994) Organization of projections from the ventromedial nucleus of the hypothalamus: A Phaseolus vulgaris - leucoagglutinin study in the rat. J Comp Neurol, 348: 41–79.
• 25. Canteras NS, Simerly RB, Swanson LW, (1995) Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol, 360: 213–245.
• 26. Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum and hypothalamus: A PHAL anterograde track-tracing study in the rat. J Comp Neurol, 324: 180–194.
• 27. Christensen M-K, Frederickson CJ (1998) Zinc-containing afferent projections to the rat corticomedial amygdaloid complex: A retrograde tracing study. J Comp Neurol, 400: 375–390.
• 28. Condé F, Maire-Lepoivre E, Audinat E, Crépel F (1995) Afferent connections of the medial frontal cortex of the rat. II Cortical and subcortical afferents. J Comp Neurol, 352: 567–593.
• 29. Cullinan WE, Herman JP, Watson JS (1993) Ventral subicular interaction with the hypothalamic paraventricular nucleus: Evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol, 332: 1–20.
• 30. Danielson EH, Magnuson DJ, Gray TS (1989) The central amygdaloid nucleus innervation of the dorsal vagal complex in rat: A Phaseolus vulgaris, leucoagglutinin lectin anterograde tracing study. Brain Res Bull, 22: 705–715.
• 31. Datta S, Siwek F, Patterson EH, Cipolloni PB (1998) Localization of pontine PGO wave generation sites and their anatomical projections in the rat. Synapse, 30: 409–423.
• 32. Davis M (1992) The role of the amygdala in conditioned fear. In: Aggleton JP (ed.). The amygdala: Neurobiological aspects of emotion, memory and mental dysfuction. Wiley-Liss Publishers, New York, pp. 255–306.
• 33. Deacon TW, Eichenbaum H, Rosenberg P, Eckmann KW (1983) Afferent connections of the perirhinal cortex in the rat. J Comp Neurol, 220: 168–190.
• 34. Gallagher M, Holland PC (1994) The amygdala complex: Multiple roles in associative learning and attention. Proc Natl Acad Sci USA, 91: 11771–11776.
• 35. Gray TS (1990) The organization and possible function of amygdaloid corticotropin-releasing factor pathways. In: De Souza EB, Nemeroff CB (eds.). Corticotropin-releasing factor: basic and clinical studies of a neuropeptide. CRC Press, Inc., Florida.
• 36. Gray TS, Carney ME, Magnuson DJ (1989) Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: Possible role in stress-induced adrenocorticotropin release. Neuroendocrinology, 50: 433–466.
• 37. Grove EA (1988a) Neural associations of the substantia innominata in the rat: Afferent connections. J Comp Neurol, 277: 315–346.
• 38. Grove EA (1988b) Efferent connections of the substantia innominata in the rat. J Comp Neurol, 277: 347–364.
• 39. Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol, 308: 249–276.
• 40. Insausti R, Herrero MT, Witter MP (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions andthe origin and distribution of cortical efferents. Hippocampus, 7: 146–183.
• 41. Jolkkonen E, Pitkänen A (1998a) Intrinsic connections of the rat amygdaloid complex: projections originating in the central nucleus. J Comp Neurol, 395: 53–72.
• 42. Jolkkonen E, Pitkänen A (1998b) Projections from the amygdalapiriform transition area to the central nucleus of the amygdala: A PHA-L study in the rat. Soc Neurosci Abstr, 24: 675.
• 43. Kelley AE, Domensick VB, Nauta WJH (1982) The amygdalostriatal projection in the rat - an anatomical study by anterograde and retrograde tracing methods. Neuroscience, 7: 615–630.
• 44. Kemppainen S, Pitkänen A (1998) Projections from the posterior cortical nucleus of the amygdala to other temporal lobe areas in rat. Soc Neurosci Abstr, 24: 676.
• 45. Kirouac GJ, Ganguly PK (1995) Topographical organization in the nucleus accumbens of afferents from the basolateral amygdala and efferents to the lateral hypothalamus. Neuroscience, 67: 625–630.
• 46. Kita H, Kitai ST (1990) Amygdaloid projections to the frontal cortex and the striatum in the rat. J Comp Neurol, 298: 40–49.
• 47. Kita H, Oomura Y (1982) An HRP study of the afferent connections of the rat lateral hypothalamic region. Brain Res Bull, 8: 63–71.
• 48. Krettek JE, Price JL (1974) Projections from the amygdala to the perirhinal and entrorhinal cortices and the subiculum. Brain Res, 71: 150–154.
• 49. Krettek JE, Price JL (1977a) Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J Comp Neurol, 172: 687–722.
• 50. Krettek JE, Price JL (1977b) Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat. J Comp Neurol, 172: 723–752.
• 51. Krettek JE, Price JL (1978a) Amygdaloid projections to subcortical structures in the basal forebrain and brainstem in the rat and cat. J Comp Neurol, 178: 225–254.
• 52. Krettek JE, Price JL (1978b) A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol, 178: 255–280.
• 53. Krieger MS, Conrad LCA, Pfaff DW (1979) An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. J Comp Neurol, 183: 785–816.
• 54. Krukoff TL, Harris KH, Jhamandas JH (1993) Efferent projections from the parabrachial nucleus demonstrated with anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res Bull, 30: 163–172.
• 55. LaBar KS, LeDoux JE, Spencer DD, Phelps EA (1995) Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci, 15: 6846–6855.
• 56. LeDoux JE (1992) Emotion and the amygdala. In: Aggleton JP (ed.). The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction. WileyLiss Publishers, New York, pp. 339–352.
• 57. LeDoux JE, Farb C, Ruggiero DA (1990) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci, 10: 1043–1054.
• 58. LeDoux JE, Farb C, Romanski LM (1991) Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci Lett, 134: 139–144.
• 59. Linke R, de Lima AD, Schwegler H, Pape H-C (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.
• 60. Luiten PGM, Spencer DG Jr, Traber J, Gaykema RPA (1985) The pattern of cortical projections from the intermediate parts of the magnocellular nucleus basalis in the rat demonstrated by tracing with Phaseolus vulgaris-leucoagglutinin. Neurosci Lett, 57: 137–142.
• 61. Luskin MB, Price JL (1983a) The topographic organization of associational fibres of the olfactory system in the rat, including centrifugal fibres to the olfactory bulb. J Comp Neurol, 216: 264–291.
• 62. Luskin MB, Price JL (1983b) The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol, 216: 292–302.
• 63. Maquet P, Peters J, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1996) Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature, 383: 163–166.
• 64. Mascagni F, McDonald AJ, Coleman JR (1993) Corticoamygdaloid and corticocortical projections of the rat temporal cortex: a Phaseolus vulgaris leucoagglutinin study. Neuroscience, 57: 697–715.
• 65. McDonald AJ (1987a) Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: A fluorescence retrograde transport study in the rat. J Comp Neurol, 262: 46–58.
• 66. McDonald AJ (1987b) Somatostatinergic projections from the amygdala to the bed nucleus of the stria terminalis and medial preoptic-hypothalamic region. Neurosci Lett, 75: 271–277.
• 67. McDonald AJ (1991a) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience, 44: 1–14.
• 68. McDonald AJ (1991b) Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens and related striatal-like areas of the rat brain. Neuroscience, 44: 15–33.
• 69. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol, 55: 257–332.
• 70. McDonald AJ, Jackson TR (1987) Amygdaloid connections with posterior insular and temporal cortical areas in the rat. J Comp Neurol, 262: 59–77.
• 71. McDonald AJ, Mascagni F (1996) Cortico-cortical and cortico-amygdaloid projections of the rat occipital cortex: A phaselous vulgaris leucoagglutinin study. Neuroscience, 71: 37–54.
• 72. McDonald AJ, Mascagni F (1997) Projections of the lateral entorhinal cortex to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience, 77: 445–460.
• 73. McDonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience, 71: 55–75.
• 74. McIntyre DC, Kelly ME, Staines WA (1996) Efferent projections of the anterior perirhinal cortex in the rat. J Comp Neurol, 396: 302–318.
• 75. Millhouse OE, Uemura-Sumi M (1985) The structure of the nucleus of the lateral olfactory tract. J Comp Neurol, 233: 517–552.
• 76. Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol, 359: 221–238.
• 77. Morris JS, Öhman A, Dolan RJ (1998) Conscious and unconscious emotional learning in the human amygdala. Nature, 393: 467–470.
• 78. Namura S, Takada M, Kikuchi H, Mizuno N (1997) Collateral projections of single neurons in the posterior thalamic region to both the temporal cortex and the amygdala: A fluorescent retrograde double-labeling study in the rat. J Comp Neurol, 384: 59–70.
• 79. Nitecka L (1981) Connections of the hypothalamus and preoptic area with nuclei of the amygdaloid body in the rat: HRP retrograde transport study. Acta Neurobiol Exp, 41: 53–67.
• 80. Nitecka L, Amerski L, Panek-Mikuza J, Narkiewicz O (1979) Thalamoamygdaloid connections studied by the method of retrograde transport. Acta Neurobiol Exp, 39: 585–601.
• 81. Nitecka L, Amerski, L, Panek-Mikula J, Narkiewicz O (1980) Tegmental afferents of the amygdaloid body in the rat. Acta Neurobiol Exp, 40: 609–624.
• 82. de Olmos J, Hardy H, Heimer L (1978) The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J Comp Neurol, 181: 213–244.
• 83. de Olmos J, Alheid GF, Beltramino CA (1985) Amygdala. In: Paxinos G (ed.). The rat nervous system. Academic Press, Sydney.
• 84. Ono T, Luiten PGM, Nishijo H, Fukuda M, Nishino H (1985) Topographic organization of projections from the amygdala to the hypothalamus of the rat. Neurosci Res, 2: 221–239.
• 85. Ottersen OP (1980) Afferent connections to the amygdaloid complex of the rat and cat: II. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol, 194: 267–289.
• 86. 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.
• 87. Ottersen OP (1982) Connections of the amygdala of the rat. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol, 205: 30–48.
• 88. Ottersen OP, Ben-Ari Y (1979) Afferent connections to the amygdaloid complex of the rat and cat. J Comp Neurol, 187: 401–424.
• 89. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, New York.
• 90. Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol, 374: 387–420.
• 91. Petrovich GD, Swanson LW (1997) Projections from the lateral part of the central amygdalar nucleus to the postulated fear conditioning circuit. Brain Research, 763: 247–254.
• 92. Phillips RG, LeDoux JE (1992) Overlapping and divergent projections of CA1 and ventral subiculum to the amygdala. Soc Neurosci Abstr, 18: 518.
• 93. Pickel VM, Van Bockstaele JC, Chan J, Cestari DM (1995) Amygdala efferents from inhibitory-type synapses with a subpopulation of catecholaminergic neurons in the rat nucleus tractus solitarius. J Comp Neurol, 362: 510–523.
• 94. Pikkarainen M, Rönkkö S, Savander V, Insausti R, Pitkänen A (1999) Projections from the lateral, basal and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol, 403: 229–260.
• 95. Pitkänen A (2000) Connectivity of the rat amygdaloid complex. In: Aggleton JP (ed.). The amygdala: a functional analysis. Oxford University Press.
• 96. Pitkänen A, Savander V, LeDoux JE (1997) Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci, 20: 517–523.
• 97. Pitkänen A, Tuunanen J, Kälviäinen R, Partanen K, Salmenperä T (1998) Amygdala damage in experimental and human epilepsy. Epilepsy Res, 328: 233–253.
• 98. Post S, Mai JK (1978) Evidence for amygdaloid projections to the contralateral hypothalamus and the ipsilateral midbrain in the rat. Cell Tissue Res, 191: 183–186.
• 99. Post S, Mai JK (1980) Contribution to the amygdaloid projection field in the rat. A quantitative autoradiographic study. J Hirnforsch, 21: 199–225.
• 100. Prewitt CMF, Herman JP (1998) Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J Chem Neuroanat, 15: 173–185.
• 101. Price JL (1973) An autoradiographic study of complementary laminar patterns of termination of afferent fibres to the olfactory cortex. J Comp Neurol, 15: 87–108.
• 102. Price JL, Russchen FT, Amaral DG (1987) Integrated systems of the CNS. The Limbic Region. II: The Amygdaloid Complex. In: Björklund A, Hökfelt T, Swanson LW (eds.). Handbook of chemical neuroanatomy. Vol. 5., Part I. Elsevier, Amsterdam.
• 103. Price JL, Slotnik BM, Revial M (1991) Olfactory projections to the hypothalamus. J Comp Neurol, 306: 447–461.
• 104. Rauch SL, van der Kolk BA, Fisler RE, Alpert NM, Orr SP, Savage CR, Fischman AJ, Jenike MA, Pitman RK (1996) A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Arch Gen Psychiatry, 53: 380–387.
• 105. Ray JP, Price JL (1992) The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol, 323: 167–197.
• 106. Reynolds GP (1992) The amygdala and the neurochemisty of schizophrenia. In: Aggleton JP (ed.). The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction. Wiley-Liss, Inc., New York, pp. 561–574.
• 107. Risold PY, Canteras NS, Swanson LW (1994) Organization of projections from the anterior hypothalamic nucleus: A Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol, 348: 1–40.
• 108. Romanski LM, LeDoux JE (1993) Information cascade from primary auditory cortex to the amygdala: Corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cereb. Cortex, 3: 515–532.
• 109. Rosen JB, Hitchcock JM, Sanases CB, Miserendino MJD, Davis M (1991) A direct projection from the central nucleus of the amygdala to the acoustic startle pathway: Anterograde and retrograde tracing studies. Behav Neurosci, 105: 817–825.
• 110. Russchen FT, Price JL (1984) Amygdalostriatal projections in the rat. Topographical organization and fiber morphology shown using the lectin PHA-L as an anterograde tracer. Neurosci Lett, 47: 15–22.
• 111. Saper CB, Loewy AD (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res, 197: 291–317.
• 112. Sarter M, Markowitsch HJ (1983) Convergence of basolateral amygdaloid and mediodorsal thalamic projections in different areas of the frontal cortex in the rat. Brain Res Bull, 10: 607–622.
• 113. Sarter M, Markowitsch HJ (1984) Collateral innervation of the medial and lateral prefrontal cortex by amygdaloid, thalamic and brain-stem neurons. J Comp Neurol, 224: 445–460.
• 114. Savander V, Miettinen M, Rönkkö S, Pitkänen A (1997) Projections from the lateral, basal and accessory basal nuclei of the amygdala to the perirhinal and postrhinal cortices: A Phaseolus vulgaris leucoagglutinin study in rat. Soc Neurosci Abstr, 23: 2101.
• 115. Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol, 161: 31–55.
• 116. Schmued L, Phermsangngam P, Lee H, Thio S, Chen E, Truong P, Colton E, Fallon J (1989) Collateralization and GAD immunoreactivity of descending pallidal efferents. Brain Res, 487: 131–142.
• 117. Scott SK, Young AW, Calder AJ, Hellawell DJ, Aggleton JP, Johnson M (1997) Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature, 385: 254–257.
• 118. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaselous vulgaris leucoagglutinin. J Comp Neurol, 290: 213–242.
• 119. Sheline YI, Gado MH, Price JL (1998) Amygdala core nuclei volumes are decreased in recurrent major depression. Neuroreport, 9: 2023–2028.
• 120. Shi C-J, Cassell MD (1997) Cortical, thalamic and amygdaloid projections of rat temporal cortex. J Comp Neurol, 382: 153–175.
• 121. Shi C-J, Cassell MD (1998a) Cortical, thalamic and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol, 399: 440–468.
• 122. Shi C-J, Cassell MD (1998b) Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex. J Comp Neurol, 399: 469–491.
• 123. Shi C-J, Cassell MD (1999) Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat. J Comp Neurol, 406: 299–328.
• 124. Shinonaga Y, Takada M, Mizuno N (1994) Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat. Neuroscience, 58: 389–397.
• 125. Simerly RB, Swanson LW (1986) The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol, 246: 312–342.
• 126. Su H-S, Bentivoglio M (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala and hippocampus in the rat. J Comp Neurol, 297: 582–593.
• 127. Sun N, Roberts L, Cassell MD (1991) Rat central amygdaloid nucleus projections to the bed nucleus of the stria terminalis. Brain Res Bull, 27: 651–662.
• 128. Sun N, Yi H, Cassell MD (1994) Evidence for a GABAergic interface between cortical afferents and brainstem projection neurons in the rat central extended amygdala. J Comp Neurol, 340: 43–64.
• 129. Swanson LW (1992): Brain maps: structure of the rat brain. Elsevier, Amsterdam.
• 130. Swanson LW, Kohler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci, 6: 3010–3023.
• 131. Switzer RC, de Olmos J, Heimer L (1985) Olfactory system. In: G Paxinos (ed.). The Rat Nervous System. Academic Press, Sydney, pp. 1–35.
• 132. Takagishi M, Chiba T (1991) Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res, 566: 26–39.
• 133. Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala´s role in sensory processing. J Comp Neurol, 313: 295–325.
• 134. Turner BH, Zimmer J (1984) The architecture and some of the interconnections of the rat´s amygdala and lateral periallocortex. J Comp Neurol, 227: 540–557.
• 135. Van Bockstaele EJ, Chan J, Pickel VM (1996) Input from central nucleus of the amygdala efferents to pericoerulear dendrites, some of which contain tyrosine hydroxylase immunoreactivity. J Neurosci Res, 45: 289–302.
• 136. Van Groen T, Wyss JM (1990a) The connections of presubiculum and parasubiculum in the rat. Brain Res, 518: 227–243.
• 137. Van Groen T, Wyss JM (1990b) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical and bilateral hippocampal formation projections. J Comp Neurol, 302: 515–528.
• 138. Vankova M, Arluison M, Leviel V, Tramu G (1992) Afferent connections of the rat substantia nigra pars lateralis with special reference to peptide-containing neurons of the amygdalo-nigral pathway. J Chem Neuroanat, 5: 39–50.
• 139. Van Vulpen EHS, Verwer RWH (1989) Organization of projections from the mediodorsal nucleus of the thalamus to the basolateral complex of the amygdala in the rat. Brain Res, 500: 389–394.
• 140. Veening JG (1978a) Cortical afferents of the amygdaloid complex in the rat: An HRP study. Neurosci Lett, 8: 191–195.
• 141. Veening JG (1978b) Subcortical afferents of the amygdaloid complex in the rat: an HRP study. Neurosci Lett, 8: 197–202.
• 142. Vereecken THLG, Vogels OJM, Nieuwenhuys R (1994) Neuron loss and shrinkage in the amygdala in Alzheimer’s disease. Neurobiol Aging, 15: 45–54.
• 143. Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol, 313: 643–668.
• 144. Vertes RP, Crane AL, Colom LV, Bland BH (1995) Ascending projections of the posterior nucleus of the hypothalamus: PHA-L analysis in the rat. J Comp Neurol, 359: 90–116.
• 145. Wallace DM, Magnuson DJ, Gray TS (1989) The amygdalo-brainstem pathway: selective innervation of dopaminergic, noradrenergic and adrenergic cells in the rat. Neurosci Lett, 97: 252–258.
• 146. Weller KL, Smith DA (1982) Afferent connections to the bed nucleus of the stria terminals. Brain Res, 232: 255–270.
• 147. Woolf NJ, Butcher LL (1982) Cholinergic projections to the basolateral amygdala: A combined evans blue and acetylcholinesterase analysis. Brain Res Bull, 8: 751–763.
• 148. Wright C, Groenewegen HJ (1995) Patterns of convergence and segregation in the medial nucleus accumbens of the rat: Relationships of prefrontal cortical, midline thalamic and basal amygdaloid afferents. J Comp Neurol, 361: 383–403.
• 149. Wright CI, Groenewegen HJ (1996) Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat. Neuroscience, 73: 359–373.
• 150. Wright CI, Beijer AVJ, Groenewegen HJ (1996) Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci, 16: 1877–1893.
• 151. Wyss JM (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J Comp Neurol, 199: 495–512.
• 152. Yasui Y, Breder CD, Saper CB, Cechetto DF (1991) Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol, 303: 355–374.
• 153. Zald DH, Pardo JV (1997) Emotion, olfaction and the human amygdala: Amygdala activation during aversive olfactory stimulation. Neurobiology (Bp), 94: 4119–4124.