Topographic organization of neurons in the acoustic thalamus that project to the amygdala

Projections from the posterior thalamus to the amygdala have been implicated in the processing of the emotional significance of acoustic stimuli. The aim of the present studies was to determine which areas of the amygdala receive afferents from posterior thalamic structures that, in turn, receive afferents (presumably acoustic afferents) from the inferior colliculus. Projections from the posterior thalamus to the amygdala and striatum were examined in rats using anterograde and retrograde axonal transport techniques. Following injections of WGA-HRP into the posterior thalamic areas [including the medial division of the medial geniculate body, the posterior intralaminar nucleus (PIN) and the medial posterior complex (POM)], anterograde transport was seen in the lateral (AL), central (ACE), medial (AM), and basomedial (ABM) nuclei of the amygdala and in the amygdalostriatal transition area (AST) and posterior caudate putamen (CPU). Injection of WGA-HRP into each anterogradely labeled area produced retrograde transport to the posterior thalamus, but the pattern of transport varied with the site of the injection. Injections in AL and AST produced retrograde transport to neurons in the medial division of the medial geniculate body (MGM), PIN, suprageniculate nucleus (SG) and, to a lesser extent, the lateral posterior nucleus (LP). Injections of the ACE, AM, and ABM, in contrast, only labeled cells in POM. While the MGM, PIN, and SG each receive afferents from the inferior colliculus, POM does not. AL and AST, therefore, receive inputs from thalamic areas that, in turn, receive inputs from the inferior colliculus.

[1]  Joseph E. LeDoux,et al.  Sensory systems and emotion: A model of affective processing , 1986 .

[2]  J. Stein,et al.  Functional analysis of hypothalamic control of the cardiovascular responses accompanying emotional behavior. , 1980, Federation proceedings.

[3]  Joseph E LeDoux,et al.  Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat , 1985, The Journal of comparative neurology.

[4]  E. G. Jones,et al.  Midbrain, diencephalic and cortical relationships of the basal nucleus of meynert and associated structures in primates , 1976, The Journal of comparative neurology.

[5]  J. Goldberg,et al.  Projections of the inferior colliculus in the monkey. , 1966, Experimental neurology.

[6]  Joseph E LeDoux,et al.  Destruction of intrinsic neurons in the lateral hypothalamus disrupts the classical conditioning of autonomic but not behavioral emotional responses in the rat , 1986, Brain Research.

[7]  D. P. Phillips,et al.  Acoustic input to single neurons in pulvinar-posterior complex of cat thalamus. , 1979, Journal of neurophysiology.

[8]  W. Mehler Subcortical afferent connections of the amygdala in the monkey , 1980, The Journal of comparative neurology.

[9]  Michela Gallagher,et al.  Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit , 1979, Physiology & Behavior.

[10]  L. Schmued,et al.  Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties , 1986, Brain Research.

[11]  O. E. Millhouse The intercalated cells of the amygdala , 1986, The Journal of comparative neurology.

[12]  H. Burton,et al.  Cytoarchitecture and somatic sensory connectivity of thalamic nuclei other than the ventrobasal complex in the cat , 1974, The Journal of comparative neurology.

[13]  A Sakaguchi,et al.  Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  F. Ebner A COMPARISON OF PRIMITIVE FOREBRAIN ORGANIZATION IN METATHERIAN AND EUTHERIAN MAMMALS * , 1969 .

[15]  J. Haight,et al.  Neocortical projections of the suprageniculate and posterior thalamic nuclei in the marsupial brush‐tailed possum, Trichosurus vulpecula(phalangeridae), with a comparative commentary on the organization of the posterior thalamus in marsupial and placental mammals , 1983, The Journal of comparative neurology.

[16]  W. Nauta,et al.  A General Profile of the Vertebrate Brain, with Sidelights on the Ancestry of Cerebral Cortex , 1970 .

[17]  J. Winer,et al.  A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys virginiana, with a comment on the posterior intralaminar nuclei of the thalamus , 1988, The Journal of comparative neurology.

[18]  F. Ebner,et al.  Evidence for two organizational plans within the somatic sensory‐motor cortex of the rat , 1979, The Journal of comparative neurology.

[19]  Joseph E LeDoux,et al.  Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Y. Ben-Ari,et al.  Afferent connections to the amygdaloid complex of the rat and cat. I. Projections from the thalamus , 1979, The Journal of comparative neurology.

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

[22]  A. Graybiel Some ascending connections of the pulvinar and nucleus lateralis posterior of the thalamus in the cat. , 1972, Brain research.

[23]  M. Kudo,et al.  Origin of mammalian thalamocortical projections. I. Telencephalic projections of the medial geniculate body in the opossum (Didelphis virginiana) , 1986, The Journal of comparative neurology.

[24]  Joseph E LeDoux,et al.  Indelibility of Subcortical Emotional Memories , 1989, Journal of Cognitive Neuroscience.

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

[26]  L. Aitkin,et al.  Auditory forebrain organization of an australian marsupial, the northern native cat (Dasyurus hallucatus) , 1989, The Journal of comparative neurology.

[27]  F. T. Russchen,et al.  Amygdalopetal projections in the cat. II. Subcortical afferent connections. A study with retrograde tracing techniques , 1982, The Journal of comparative neurology.

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

[29]  J. Winer,et al.  The medial division of the medial geniculate body of the cat: implications for thalamic organization , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[31]  Joseph E LeDoux,et al.  Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli , 1986, Neuroscience.

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

[33]  Michael Davis,et al.  Anxiety and the Amygdala: Pharmacological and Anatomical Analysis of the Fear-Potentiated Startle Paradigm , 1988 .

[34]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[35]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[36]  Joseph E LeDoux,et al.  Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat , 1987, The Journal of comparative neurology.

[37]  N. Schneiderman,et al.  The role of amygdaloid central nucleus in the retention of differential pavlovian conditioning of bradycardia in rabbits , 1986, Behavioural Brain Research.

[38]  J. Veening Subcortical afferents of the amygdaloid complex in the rat: an HRP study , 1978, Neuroscience Letters.

[39]  Joseph E LeDoux,et al.  The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.