Cortical Afferents to the Extended Amygdala
Corresponding Author
ALEXANDER J. McDONALD
Department of Cell Biology and Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208, USA
Voice: 803-733-3378; fax: 803-733-3212; [email protected]Search for more papers by this authorSARA J. SHAMMAH-LAGNADO
Department of Physiology and Biophysics, University of São Paulo, Institute of Biomedical Science, São Paulo, SP 05508, Brazil
Search for more papers by this authorCHANGJUN SHI
Department of Psychiatry and Behavioral Science, Emory University School of Medicine, Atlanta, Georgia 30322, USA
Search for more papers by this authorMICHAEL DAVIS
Department of Psychiatry and Behavioral Science, Emory University School of Medicine, Atlanta, Georgia 30322, USA
Search for more papers by this authorCorresponding Author
ALEXANDER J. McDONALD
Department of Cell Biology and Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208, USA
Voice: 803-733-3378; fax: 803-733-3212; [email protected]Search for more papers by this authorSARA J. SHAMMAH-LAGNADO
Department of Physiology and Biophysics, University of São Paulo, Institute of Biomedical Science, São Paulo, SP 05508, Brazil
Search for more papers by this authorCHANGJUN SHI
Department of Psychiatry and Behavioral Science, Emory University School of Medicine, Atlanta, Georgia 30322, USA
Search for more papers by this authorMICHAEL DAVIS
Department of Psychiatry and Behavioral Science, Emory University School of Medicine, Atlanta, Georgia 30322, USA
Search for more papers by this authorAbstract
ABSTRACT: The projections of the cerebral cortex to the extended amygdala were studied in the rat using anterograde and retrograde tract-tracing techniques. Most cortical areas with strong projections to the extended amygdala preferentially targeted either the medial extended amygdala (including the medial amygdalar nucleus, ventromedial substantia innominata, and the medial part of the bed nucleus the stria terminalis) or the central extended amygdala (including the central amygdalar nucleus, dorsolateral substantia innominata, and the lateral part of the bed nucleus of the stria terminalis). Some cortical areas, however, had equal projections to both medial and central portions. The main areas projecting preferentially to the medial extended amygdala were the ventral subiculum, infralimbic cortex, ventral agranular insular area, and the rostral part of the ventrolateral entorhinal area. The main areas projecting preferentially to the central extended amygdala were the prefrontal cortex, viscerosensory and somatosensory portions of the insular cortex, and the amygdalopiriform transitional area. It is suggested that these cortical inputs may be important for cognitive, mnemonic, and affective aspects of emotional and motivated behavior.
REFERENCES
- 1 Heimer, L., J. de Olmos, G.F. Afheid & L. Záborsky. 1991. “Perestroika” in the basal forebrain: opening the border between neurology and psychiatry. Prog. Brain Res. 87: 109–165.
- 2 Heimer, L., R.E. Harlan, G.F. Alheid, M.M. Garcia & J. De Olmos. 1997. Substantia innominata: A notion which impedes clinical anatomical correlations in neuropsychiatric disorders. Neuroscience 76: 957–1006.
- 3 Alheid, G.F., J.S. De Olmos & C.A. Beltramino. 1995. Amygdala and extended amygdala. In The Rat Nervous System. G. Paxinos, Ed.: 495-578. Academic Press. Orlando, FL.
- 4 Holstege, G. 1992. The emotional motor system. Eur. J. Morphol. 30: 67–79.
- 5 McDonald, A.J. 1998. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55: 257–332.
- 6 McDonald, A.J. 1982. Cytoarchitecture of the central amygdaloid nucleus of the rat. J. Comp. Neurol. 208: 401–418.
- 7 Kosar, E., H.J. Grill & R. Norgren. 1986. Gustatory cortex in the rat. I: Physiological properties and cytoarchitecture. Brain Res. 379: 329–341.
- 8 Cechetto, D.F. & C.B. Saper. 1987. Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J. Comp. Neurol. 262: 27–45.
- 9
Shi, C-J. & M.D. Cassell.
1998. Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices.
J. Comp. Neurol.
399: 440–468.
10.1002/(SICI)1096-9861(19981005)399:4<440::AID-CNE2>3.0.CO;2-1 CASPubMedWeb of Science®Google Scholar
- 10 Fabri, M. & H. Burton. 1991. Ipsilateral cortical connections of primary somatic sensory cortex in rats. J. Comp. Neurol. 311: 405–424.
- 11
Shi, C-J. & M.D. Cassell.
1998. Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex.
J. Comp. Neurol.
399: 469–491.
10.1002/(SICI)1096-9861(19981005)399:4<469::AID-CNE3>3.0.CO;2-# CASPubMedWeb of Science®Google Scholar
- 12 Luskin, M.B. & J.L. Price. 1983. The topographic organization of association fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J. Comp. Neurol. 216: 264–291.
- 13 Paxinos, G. & C. Watson. 1986. The Rat Brain in Stereotaxic Coordinates. Academic Press. New York.
- 14 Krettek, J.E. & J.L. Price. 1977. Projections of the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J. Comp. Neurol. 172: 687–722.
- 15 Canteras, N.S. & L.W. Swanson. 1992. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 324: 180–194.
- 16 Cullinan, W.E., J.P. Herman & S.J. Watson. 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.
- 17 Ottersen, O.P. 1982. Connections of the amygdala of the rat. IV. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J. Comp. Neurol. 205: 30–48.
- 18 McDonald, A.J. & F. Mascagni. 1997. Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 77: 445–460.
- 19 Witter, M.O., H.J. Groenewegen, F.H. Lopes Da Silva & A.H.M. Lohman. 1989. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33: 161–253.
- 20 Hurley, K.M., H. Herbert, M.M. Moga & C.B. Saper. 1991. Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 308: 249–276.
- 21 Takagishi, M. & C. Chiba. 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.
- 22 Canteras, N.S., R.B. Simerly & L.W. Swanson. 1995. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 360: 231–245.
- 23 De Olmos, J.S., G.F Alheid & C.A. Bertramino. 1985. Amygdala. In The Rat Nervous System. G. Paxinos. Ed.: 223-334. Academic Press. Orlando.
- 24 Krettek, J.E. & J.L. Price. 1978. Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp. Neurol. 178: 225–254.
- 25 Krettek, J.E. & J.L. Price. 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.
- 26 Scalia, F. & S.S.Winans. 1975. The different projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161: 31–56.
- 27 Swanson, L.W. & W.M. Cowan. 1977. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 172: 49–84.
- 28 Luiten, P.G.M., J.M. Koolhaas, S. De Boer & S.J. Koopmans. 1985. The cortico-medial amygdala in the central nervous system organization of agonistic behavior. Brain Res. 332: 283–297.
- 29 Morgan, M.A., L.M. Romanski and J.E. Ledoux. 1993. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett. 163: 109–113.
- 30 Gray, T.S., E.C. Carney & J.M. Mangusson. 1989. Direct projections from the central amydaloid nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. Neuroendocrinology 50: 433–446.
- 31 McDonald, A.J., F. Mascagni & L. Guo. 1996. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71: 55–75.
- 32 Sesack, S.R., A.Y. Deutch, R.H. Roth & B.S. Bunney. 1989. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 209: 213–242.
- 33 McDonald, A.J. & T.R. Jackson. 1987. Amygdaloid connections with posterior insular and temporal cortical areas in the rat. J. Comp. Neurol. 262: 59–77.
- 34 Saper, C.B. 1982. Convergence of autonomic and limbic connections in the insular cortex of the rat. J. Comp. Neurol. 210: 163–173.
- 35 Yasui, Y., C.D. Breder, C.B. Saper & D.F. Cechetto. 1991. Autonomic responses and efferent pathways from the insular cortex in the rat. J. Comp. Neurol. 303: 355–374.
- 36 McDonald, A.J. 1983. Neurons of the bed nucleus of the stria terminalis: a Golgi study in the rat. Brain Res. Bull. 10: 11–120.
- 37 Davis, M. 1992. The role of the amygdala in conditioned fear. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. J.P. Aggleton, Ed.: 255-306. Wiley-Liss. New York.
- 38 Gallagher, M. & P.C. Holland. 1992. Understanding the function of the central nucleus: is simple conditioning enough?In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dusfunction. J.G. Aggleton, Ed.: 307-321. Wiley-Liss. New York.
- 39 Ledoux, J.E. 1992. Emotion and the amygdala. In The Amygdala: Neurobiological aspects of Emotion, Memory, and Mental Dysfunction. J. P. Aggleton, Ed. 339-351. Wiley-Liss. New York.
- 40 Holstege, G., L. Meiners & T. Tan. 1985. Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons and medulla oblongata in the cat. Exp. Brain Res. 58: 379–391.
- 41 Schwaber, J.S., B.S. Kapp & G. Higgins. 1980. The origin and extent of direct amygdala projections to the region of the dorsal motor nucleus of the vagus and the nucleus of the solitary tract. Neurosci. Lett. 20: 15–20.
- 42 Walker, D.L. & M. Davis. 1997. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amgydala in startle increases produced by conditioned versus unconditioned fear. J. Neurosci. 17: 9375–9383.
- 43 Alden, M., J-M. Besson & J-F. Bernard. 1994. Organization of the efferent projections from the pontine parabrachial area to the bed nucleus of the stria terminalis and neighboring regions: a PHA-L study in the rat. J. Comp. Neurol. 341: 289–314.
- 44 Bernard, J.F., M. Alden & J.M. Besson. 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.
- 45 Ricardo, J.A. & E.T. Koh. 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.
- 46 Barnett, E.M., G.D. Evans, N. Sun, S. Perlman & M.D. Cassell. 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.
- 47 Killcross, S., T.W. Robbins & B.J. Everitt. 1997. Different types of fear-conditioned behavior mediated by separate nuclei within the amygdala. Nature 388: 377–380.
- 48 Ledoux, J. 1996. The Emotional Brain. Simon and Schuster. New York.
- 49 James, W. 1884. What is emotion? Mind 19: 188–205.
- 50 Pascoe, J.P. & B.S. Kapp. 1987. Responses of amygdaloid central nucleus neurons to stimulation of the insular cortex in awake rabbits. Neuroscience 21: 471–485.
- 51 McDonald, A.J. 1991. Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44: 15–33.
- 52 Sananes, C.B. & B.A. Campbell. 1989. A role of the central nucleus of the amygdala in olfactory heart rate conditioning. Behav. Neurosci. 103: 519–525.
- 53 Mascagni, F., A.J. McDonald & J.R. Coleman. 1993. Cortico-amygdaloid and cortico-cortical projections of the rat temporal cortex: a Phaseolus vulgaris leucoagglutinin study. Neuroscience 57: 697–715.