Cortical Afferents to the Extended Amygdala

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.

[1]  A. McDonald,et al.  Neurons of the bed nucleus of the stria terminalis: A golgi study in the rat , 1983, Brain Research Bulletin.

[2]  F. Mascagni,et al.  Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat , 1997, Neuroscience.

[3]  J. Price,et al.  A description of the amygdaloid complex in the rat and cat with observations on intra‐amygdaloid axonal connections , 1978, The Journal of comparative neurology.

[4]  P. Holland,et al.  Understanding the function of the central nucleus: Is simple conditioning enough? , 1992 .

[5]  B. Campbell,et al.  Role of the central nucleus of the amygdala in olfactory heart rate conditioning. , 1989, Behavioral neuroscience.

[6]  G. Alheid Amygdala and extended amygdala , 1995 .

[7]  B. Kapp,et al.  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 , 1980, Neuroscience Letters.

[8]  W. James II.—WHAT IS AN EMOTION ? , 1884 .

[9]  A. McDonald,et al.  Amygdaloid connections with posterior insular and temporal cortical areas in the rat , 1987, The Journal of comparative neurology.

[10]  L. Swanson,et al.  Organization of projections from the basomedial nucleus of the amygdala: A PHAL study in the rat , 1996, The Journal of comparative neurology.

[11]  C. Saper,et al.  Efferent projections of the infralimbic cortex of the rat , 1991, The Journal of comparative neurology.

[12]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[13]  Michael Davis,et al.  Double Dissociation between the Involvement of the Bed Nucleus of the Stria Terminalis and the Central Nucleus of the Amygdala in Startle Increases Produced by Conditioned versus Unconditioned Fear , 1997, The Journal of Neuroscience.

[14]  Joseph E. LeDoux,et al.  Extinction of emotional learning: Contribution of medial prefrontal cortex , 1993, Neuroscience Letters.

[15]  J. Price,et al.  Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat , 1977, The Journal of comparative neurology.

[16]  L. Heimer,et al.  "Perestroika" in the basal forebrain: opening the border between neurology and psychiatry. , 1991, Progress in brain research.

[17]  A. McDonald Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[18]  J. Koolhaas,et al.  The cortico-medial amygdala in the central nervous system organization of agonistic behavior , 1985, Brain Research.

[19]  T. Robbins,et al.  Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala , 1997, Nature.

[20]  L. Swanson,et al.  Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat , 1995, The Journal of comparative neurology.

[21]  D. Cechetto,et al.  Autonomic responses and efferent pathways from the insular cortex in the rat , 1991, The Journal of comparative neurology.

[22]  H. Grill,et al.  Gustatory cortex in the rat. I. Physiological properties and cytoarchitecture , 1986, Brain Research.

[23]  J. Besson,et al.  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 , 1994, The Journal of comparative neurology.

[24]  J. Herman,et al.  Ventral subicular interaction with the hypothalamic paraventricular nucleus: Evidence for a relay in the bed nucleus of the stria terminalis , 1993, The Journal of comparative neurology.

[25]  A. McDonald,et al.  Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain , 1991, Neuroscience.

[26]  S. S. Winans,et al.  The differential projections of the olfactory bulb and accessory olfactory bulb in mammals , 1975, The Journal of comparative neurology.

[27]  Tanemichi Chiba,et al.  Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study , 1991, Brain Research.

[28]  J. Price,et al.  Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat , 1978, The Journal of comparative neurology.

[29]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[30]  T. Gray,et al.  Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. , 1989, Neuroendocrinology.

[31]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices , 1998, The Journal of comparative neurology.

[32]  Joseph E. LeDoux,et al.  Emotion and the amygdala. , 1992 .

[33]  A. McDonald,et al.  Cytoarchitecture of the central amygdaloid nucleus of the rat , 1982, The Journal of comparative neurology.

[34]  M. Luskin,et al.  The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb , 1983, The Journal of comparative neurology.

[35]  G. Holstege,et al.  The emotional motor system. , 1992, European journal of morphology.

[36]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

[37]  C. Saper,et al.  Convergence of autonomic and limbic connections in the insular cortex of the rat , 1982, The Journal of comparative neurology.

[38]  M. Cassell,et al.  Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex , 1998, The Journal of comparative neurology.

[39]  Michael Davis,et al.  The role of the amygdala in conditioned fear. , 1992 .

[40]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[41]  L. Swanson,et al.  Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: A PHAL anterograde tract‐tracing study in the rat , 1992, The Journal of comparative neurology.

[42]  B. Kapp,et al.  Responses of amygdaloid central nucleus neurons to stimulation of the insular cortex in awake rabbits , 1987, Neuroscience.

[43]  L. Heimer,et al.  Substantia innominata: a notion which impedes clinical–anatomical correlations in neuropsychiatric disorders , 1997, Neuroscience.

[44]  C. Saper,et al.  Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat , 1987, The Journal of comparative neurology.

[45]  O. Ottersen,et al.  Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase , 1982, The Journal of comparative neurology.

[46]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[47]  F. Mascagni,et al.  Corticoamygdaloid and corticocortical projections of the rat temporal cortex: APhaseolus vulgaris leucoagglutinin study , 1993, Neuroscience.

[48]  F. Mascagni,et al.  Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat , 1996, Neuroscience.

[49]  Michael Davis,et al.  Sensitization of the startle reflex by footshock: blockade by lesions of the central nucleus of the amygdala or its efferent pathway to the brainstem. , 1989, Behavioral neuroscience.

[50]  S. Perlman,et al.  Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  Mara Fabri,et al.  Ipsilateral cortical connections of primary somatic sensory cortex in rats , 1991, The Journal of comparative neurology.

[52]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[53]  J. Besson,et al.  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 , 1993, The Journal of comparative neurology.

[54]  J. A. Ricardo,et al.  Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat , 1978, Brain Research.