Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study

We have previously described the origins of neocortical inputs to the lateral nucleus of the macaque monkey amygdala based on retrograde tracing studies. Here we report results from studies that have attempted to confirm the projections from several candidate afferent regions using 3H‐amino acid autoradiography as an anterograde tracer. We have charted, based on the results of 33 separate injections, the topographic distribution of cortical projections throughout the amygdala. Areas TE and TEO of the inferotemporal cortex, portions of the superior temporal gyrus, and the granular region of the insula project primarily to the lateral nucleus, with little or no innervation of other amygdaloid nuclei. In contrast, orbitofrontal, medial prefrontal, and anterior cingulate regions project primarily to the basal and accessory basal nuclei and provide little innervation to the lateral nucleus. The orbitofrontal and medial prefrontal cortices, but not the anterior cingulate cortex, project to medially situated amygdaloid areas such as the cortical and medial nuclei and to the periamygdaloid cortex. The agranular and dysgranular insula, the parainsula, and rostral portions of the superior temporal gyrus project both to the lateral, basal, and accessory basal nuclei and to the medially situated nuclei. Projections to the central nucleus are particularly prominent from these regions. These data are discussed in relation to the hierarchical processing of sensory information that occurs within the amygdaloid complex. J. Comp. Neurol. 451:301–323, 2002. © 2002 Wiley‐Liss, Inc.

[1]  S. Shelton,et al.  The Primate Amygdala Mediates Acute Fear But Not the Behavioral and Physiological Components of Anxious Temperament , 2001, The Journal of Neuroscience.

[2]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[4]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

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

[6]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[7]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[8]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[9]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[10]  R. E. Passingham,et al.  Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta) , 1980, Brain Research.

[11]  J. Aggleton A description of intra-amygdaloid connections in old world monkeys , 2004, Experimental Brain Research.

[12]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[13]  W. Cowan,et al.  A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[14]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[15]  D. Pandya,et al.  Efferent connections of the cingulate gyrus in the rhesus monkey , 1981, Experimental Brain Research.

[16]  B. Vogt,et al.  Chapter VIII Primate cingulate cortex chemoarchitecture and its disruption in Alzheimer's disease , 1997 .

[17]  David P. Friedman,et al.  Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch , 1986, The Journal of comparative neurology.

[18]  M Mishkin,et al.  Organization of the amygdalopetal projections from modality‐specific cortical association areas in the monkey , 1980, The Journal of comparative neurology.

[19]  D. R. Snyder,et al.  Alterations in aversive and aggressive behaviors following orbital frontal lesions in rhesus monkeys. , 1972, Acta neurobiologiae experimentalis.

[20]  T. Aoe [Retrograde transport]. , 2004, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[21]  A. Hendrickson,et al.  The autoradiographic demonstration of axonal connections in the central nervous system. , 1972, Brain research.

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

[23]  M. Yukie,et al.  Amygdalofugal and amygdalopetal connections with modality‐specific visual cortical areas in macaques (macaca fuscata, M. mulatta, and M. fascicularis) , 1987, The Journal of comparative neurology.

[24]  D. Amaral,et al.  An autoradiographic study of the projections of the central nucleus of the monkey amygdala , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  D. Amaral,et al.  Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala: A retrograde tracing study , 2000, The Journal of comparative neurology.

[26]  H. Burton,et al.  Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates , 1976, The Journal of comparative neurology.

[27]  D. Amaral,et al.  Organization of the intrinsic connections of the monkey amygdaloid complex: Projections originating in the lateral nucleus , 1998, The Journal of comparative neurology.

[28]  K Cheng,et al.  Organization of Corticostriatal and Corticoamygdalar Projections Arising from the Anterior Inferotemporal Area TE of the Macaque Monkey: A Phaseolus vulgaris Leucoagglutinin Study , 1997, The Journal of Neuroscience.

[29]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[30]  H. Teuber,et al.  Unity and diversity of frontal lobe functions. , 1972, Acta neurobiologiae experimentalis.

[31]  G. V. Hoesen,et al.  Temporal neocortical afferent connections to the amygdala in the rhesus monkey , 1976, Brain Research.

[32]  M Meunier,et al.  Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys , 1999, The European journal of neuroscience.

[33]  N. Alpert,et al.  Activation of anterior paralimbic structures during guilt-related script-driven imagery , 2000, Biological Psychiatry.

[34]  D. Rosene,et al.  A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. , 1986, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[35]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[36]  D. Pandya,et al.  Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern , 1973, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[37]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[38]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[39]  W. Nauta,et al.  Subcortical projections from the temporal neocortex in Macaca mulatta , 1956 .

[40]  N J Emery,et al.  The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta). , 2001, Behavioral neuroscience.

[41]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: I. Three‐dimensional and cytoarchitectonic organization , 2000, The Journal of comparative neurology.

[42]  D. Amaral,et al.  Cholinergic innervation of the monkey amygdala: An immunohistochemical analysis with antisera to choline acetyltransferase , 1989, The Journal of comparative neurology.

[43]  R. Myers,et al.  Neural control of social behavior: prefrontal and anterior temporal cortex. , 1973, Neuropsychologia.

[44]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[45]  A. Chiba,et al.  The amygdala and emotion , 1996, Current Opinion in Neurobiology.

[46]  B. Kaada Stimulation and Regional Ablation of the Amygdaloid Complex with Reference to Functional Representations , 1972 .

[47]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[48]  D. Amaral,et al.  An air pressure system for the injection of tracer substances into the brain , 1983, Journal of Neuroscience Methods.

[49]  A. Young,et al.  Impaired recognition and experience of disgust following brain injury , 2000, Nature Neuroscience.

[50]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TE and TEO with medial temporal- lobe structures in infant and adult monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[52]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[53]  David G. Amaral,et al.  The role of the amygdala in primate social cognition. , 2000 .

[54]  The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta). , 2001 .

[55]  D. N. Pandya,et al.  Insular interconnections with the amygdala in the rhesus monkey , 1981, Neuroscience.

[56]  David G. Amaral,et al.  The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety , 2002, Biological Psychiatry.

[57]  D. Amaral,et al.  Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys , 1996, The Journal of comparative neurology.