Cells in the posterior thalamus project to both amygdala and temporal cortex: A quantitative retrograde double‐labeling study in the rat

Auditory information from the posterior thalamus reaches the lateral nucleus of the amygdala (LA) by way of two pathways: a direct thalamo‐amygdala projection and a polysynaptic thalamo‐cortico‐amygdala projection. However, the quantitative extent of thalamic neurons that project to the LA or to the auditory association cortex (AAC) is not known. Furthermore, the extent and topographical distribution of bifurcating cells that project to both LA and AAC are also unknown. Therefore, separate tracers were injected into LA and either into all of AAC or within discrete regions of AAC, such as temporal areas TE3 or perirhinal cortex (PRh), and quantitative analyses were performed on labeling within the subregions of the auditory thalamus in rats. Following LA injections, retrogradely labeled cells were most numerous in the posterior intralaminar nucleus (PIN; 48.0% of all labeled thalamic cells), whereas labeled cells following injections of the entire AAC were most numerous in the dorsal division of the medial geniculate nucleus (MGd; 32.9% of all labeled thalamic cells). Following AAC injections localized to only TE3, the MGd again had the majority of labeled cells (35.9%), whereas following AAC injections localized to PRh, the PIN had the most labeled cells (32.8%). Double‐labeled cells were found in all the thalamic regions studied and were most commonly observed in the PIN (43.7% of all double‐labeled cells following injections into LA and throughout the AAC). The percentage of double‐labeled cells as a proportion of either LA‐projecting or AAC‐projecting cells varied among the thalamic nuclei studied, ranging from 2.9% up to 42.4%. The topographic distribution of double‐labeled cells in the thalamic nuclei resembled that of single‐labeled cells following LA injections more than single‐labeled cells following AAC injection. These findings suggest that double‐labeled cells contribute substantially to many of the direct thalamo‐amygdala and indirect thalamo‐AAC‐amygdala projections. Among other functions, these bifurcating cells may help regulate the processing of input to the LA arriving from these two pathways to allow for certain types of plasticity in the LA during fear conditioning. J. Comp. Neurol. 425:257–274, 2000. © 2000 Wiley‐Liss, Inc.

[1]  M. Davis,et al.  Lesions of the perirhinal cortex but not of the frontal, medial prefrontal, visual, or insular cortex block fear-potentiated startle using a visual conditioned stimulus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  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.

[3]  N. Mizuno,et al.  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 , 1997, The Journal of comparative neurology.

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

[5]  J. Kelly,et al.  Organization of auditory cortex in the albino rat: sound frequency. , 1988, Journal of neurophysiology.

[6]  Joseph E LeDoux,et al.  Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways. , 1996, Learning & memory.

[7]  J. Edeline Frequency-specific plasticity of single unit discharges in the rat medial geniculate body , 1990, Brain Research.

[8]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

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

[10]  J. Winer,et al.  Origins of medial geniculate body projections to physiologically defined zones of rat primary auditory cortex , 1999, Hearing Research.

[11]  D. Pandya,et al.  Corticothalamic connections of extrastriate visual areas in rhesus monkeys , 2022 .

[12]  J. Rosenblatt,et al.  Lateral habenula neurons are necessary for the hormonal onset of maternal behavior and for the display of postpartum estrus in naturally parturient female rats. , 1995, Behavioral neuroscience.

[13]  D. Price,et al.  A modified histochemical technique to visualize acetylcholinesterase-containing axons. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[14]  W. C. Hall,et al.  Nonintralaminar thalamostriatal projections in the gray squirrel (Sciurus carolinensis) and tree shrew (Tupaia glis) , 1984, The Journal of comparative neurology.

[15]  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.

[16]  J. Coleman,et al.  Anatomy of the rat medial geniculate body: I. Cytoarchitecture, myeloarchitecture, and neocortical connectivity , 1990, The Journal of comparative neurology.

[17]  D. Pandya,et al.  Corticostriatal connections of extrastriate visual areas in rhesus monkeys , 1997, The Journal of comparative neurology.

[18]  R. Linke Organization of projections to temporal cortex originating in the thalamic posterior intralaminar nucleus of the rat , 1999, Experimental Brain Research.

[19]  H. Killackey,et al.  Differential telencephalic projections of the medial and ventral divisions of the medial geniculate body of the rat. , 1974, Brain research.

[20]  H. Hughes,et al.  Anatomical and neurobehavioral investigations concerning the thalamo‐cortical organization of the rat's visual system , 1977, The Journal of comparative neurology.

[21]  M. Herkenham,et al.  Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing , 1991, The Journal of comparative neurology.

[22]  Joseph E LeDoux,et al.  Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: contributions of contextual cues. , 1995, Behavioral neuroscience.

[23]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[24]  J. Price Prefrontal Cortical Networks Related to Visceral Function and Mood , 1999, Annals of the New York Academy of Sciences.

[25]  Joseph E LeDoux Brain mechanisms of emotion and emotional learning , 1992, Current Biology.

[26]  C. Henkel,et al.  The superior colliculus control of pinna movements in the cat: Possible anatomical connections , 1978, The Journal of comparative neurology.

[27]  M. Roger,et al.  Anatomical study of the connections of the primary auditory area in the rat , 1989, The Journal of comparative neurology.

[28]  D. Sparks,et al.  Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. , 1996, Journal of neurophysiology.

[29]  G. Groos,et al.  Cortico-recipient and tecto-recipient visual zones in the rat's lateral posterior (pulvinar) nucleus: An anatomical study , 1981, Neuroscience Letters.

[30]  S. Brandner,et al.  The projection from medial geniculate to field AI in cat: organization in the isofrequency dimension , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  E. Welker,et al.  Morphology of corticothalamic terminals arising from the auditory cortex of the rat: A Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study , 1991, Hearing Research.

[32]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat , 1983, The Journal of comparative neurology.

[33]  J. K. Harting,et al.  Auditory pathways to the cortex in Tupaia glis , 1976, The Journal of comparative neurology.

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

[35]  T. Imig,et al.  Tonotopic organization in ventral nucleus of medial geniculate body in the cat. , 1985, Journal of neurophysiology.

[36]  J. Coleman,et al.  Extrastriate projections from thalamus to posterior occipital-temporal cortex in rat , 1980, Brain Research.

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

[38]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid projections of rat temporal cortex , 1997, The Journal of comparative neurology.

[39]  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.

[40]  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.

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

[42]  Joseph E LeDoux,et al.  Distinct populations of NMDA receptors at subcortical and cortical inputs to principal cells of the lateral amygdala. , 1999, Journal of neurophysiology.

[43]  Joseph E LeDoux,et al.  Topographic organization of neurons in the acoustic thalamus that project to the amygdala , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  M. Cassell,et al.  Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat , 1999, The Journal of comparative neurology.

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

[46]  K. Niimi,et al.  Projections of the medial geniculate nucleus to layer 1 of the auditory cortex in the cat traced with horseradish peroxidase , 1984, Neuroscience Letters.

[47]  G. Ring,et al.  Projections of nucleus caudalis and spinal cord to rrainstem and diencephalon in the hedgehog (Erinaceus europaeus and Paraechinus aethiopicus): A degeneration study , 1983, The Journal of comparative neurology.

[48]  Joseph E LeDoux,et al.  Organization of rodent auditory cortex: anterograde transport of PHA-L from MGv to temporal neocortex. , 1993, Cerebral cortex.

[49]  B E Stein,et al.  Control of pinna movements and sensorimotor register in cat superior colliculus. , 1981, Brain, behavior and evolution.

[50]  C Bucherelli,et al.  Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat , 1999, The Journal of Neuroscience.

[51]  D. Pandya,et al.  Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: A study with a new method for horseradish peroxidase histochemistry , 1977, Brain Research.

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

[53]  W. Krieg Connections of the cerebral cortex I. The Albino Rat. C. Extrinsic connections , 1947 .

[54]  K. Tanaka,et al.  Divergent Projections from the Anterior Inferotemporal Area TE to the Perirhinal and Entorhinal Cortices in the Macaque Monkey , 1996, The Journal of Neuroscience.

[55]  C. Saper Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus , 1984, The Journal of comparative neurology.

[56]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[57]  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.

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

[59]  O D Creutzfeldt,et al.  Anatomy of the auditory thalamocortical system of the guinea pig , 1989, The Journal of comparative neurology.

[60]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

[61]  H Eichenbaum,et al.  Afferent connections of the perirhinal cortex in the rat , 1983, The Journal of comparative neurology.

[62]  M. Takada The lateroposterior thalamic nucleus and substantia nigra pars lateralis: Origin of dual innervation over the visual system and basal ganglia , 1992, Neuroscience Letters.

[63]  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.

[64]  J. Winer,et al.  Subdivisions of the auditory cortex of the cat: The retrograde transport of horseradish peroxidase to the medial geniculate body and posterior thalamic nuclei , 1977, The Journal of comparative neurology.

[65]  D. Paré,et al.  Thalamic collaterals of corticostriatal axons: Their termination field and synaptic targets in cats , 1996, The Journal of comparative neurology.

[66]  Michael Davis,et al.  Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear- potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  Joseph E LeDoux,et al.  Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat , 1999, The Journal of comparative neurology.

[68]  Steiner Be,et al.  Control of pinna movements and sensorimotor register in cat superior colliculus. , 1981 .

[69]  Joseph E LeDoux Emotion: clues from the brain. , 1995, Annual review of psychology.

[70]  T. Hattori,et al.  Pyramidal cells in rat temporoauditory cortex project to both striatum and inferior colliculus , 1991, Brain Research Bulletin.

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

[72]  D. W. Vaughan,et al.  Thalamic and callosal connections of the rat auditory cortex , 1983, Brain Research.

[73]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the cat , 1983, The Journal of comparative neurology.

[74]  J. Winer,et al.  Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: Study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body , 1987, The Journal of comparative neurology.

[75]  M. Deschenes,et al.  A Single‐cell Study of the Axonal Projections Arising from the Posterior Intralaminar Thalamic Nuclei in the Rat , 1996, The European journal of neuroscience.

[76]  H. Pape,et al.  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 , 1999, The Journal of comparative neurology.

[77]  Joseph E. LeDoux,et al.  Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex , 1991, Neuroscience Letters.

[78]  Yasushi Miyashita,et al.  Consolidation of Visual Associative Long-Term Memory in the Temporal Cortex of Primates , 1998, Neurobiology of Learning and Memory.

[79]  Joseph E LeDoux Emotion, memory and the brain. , 1994, Scientific American.

[80]  J. Winer,et al.  Layer V in rat auditory cortex: Projections to the inferior colliculus and contralateral cortex , 1988, Hearing Research.

[81]  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 .

[82]  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.

[83]  M. Roger,et al.  Ventral temporal cortex in the rat: Connections of secondary auditory areas Te2 and Te3 , 1990, The Journal of comparative neurology.

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

[85]  W. C. Hall,et al.  The medial geniculate body of the tree shrew, Tupaia glis II. Connections with the neocortex , 1978, The Journal of comparative neurology.