Projections from the amygdaloid complex to the claustrum and the endopiriform nucleus: A Phaseolus vulgaris leucoagglutinin study in the rat

The claustrum and the endopiriform nucleus contribute to the spread of epileptiform activity from the amygdala to other brain areas. Data of the distribution of pathways underlying the information flow between these regions are, however, incomplete and controversial. To investigate the projections from the amygdala to the claustrum and the endopiriform nucleus, we injected the anterograde tracer Phaseolus vulgaris leucoagglutinin into various divisions of the amygdaloid complex, including the lateral, basal, accessory basal, central, anterior cortical and posterior cortical nuclei, the periamygdaloid cortex, and the amygdalohippocampal area in the rat. Analysis of immunohistochemically processed sections reveal that the heaviest projections to the claustrum originate in the magnocellular division of the basal nucleus. The projection is moderate in density and mainly terminates in the dorsal aspect of the anterior part of the claustrum. Light projections from the parvicellular and intermediate divisions of the basal nucleus terminate in the same region, whereas light projections from the accessory basal nucleus and the lateral division of the amygdalohippocampal area innervate the caudal part of the claustrum. The most substantial projections from the amygdala to the endopiriform nucleus originate in the lateral division of the amygdalohippocampal area. These projections terminate in the central and caudal parts of the endopiriform nucleus. Lighter projections originate in the anterior and posterior cortical nuclei, the periamygdaloid cortex, the medial division of the amygdalohippocampal area, and the accessory basal nucleus. These data provide an anatomic basis for recent functional studies demonstrating that the claustrum and the endopiriform nucleus are strategically located to synchronize and spread epileptiform activity from the amygdala to the other brain regions. These topographically organized pathways also provide a route by means of which the claustrum and the endopiriform nucleus have access to inputs from the amygdaloid networks that process emotionally significant information. J. Comp. Neurol. 451:236–249, 2002. © 2002 Wiley‐Liss, Inc.

[1]  J. Wada,et al.  Role of the Claustrum in Convulsive Evolution of Visual Afferent and Partial Nonconvulsive Seizure in Primates , 1997, Epilepsia.

[2]  J. Price,et al.  Amygdalostriatal projections in the rat. Topographical organization and fiber morphology shown using the lectin PHA-L as an anterograde tracer , 1984, Neuroscience Letters.

[3]  M. Witter,et al.  Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents , 1998, Hippocampus.

[4]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[5]  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.

[6]  E. Audinat,et al.  Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents , 1995, The Journal of comparative neurology.

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

[8]  A. Pitkänen,et al.  Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat , 1999, The Journal of comparative neurology.

[9]  M. Meredith.  Vomeronasal organ removal before sexual experience impairs male hamster mating behavior , 1986, Physiology & Behavior.

[10]  M J Campbell,et al.  An immunohistochemical characterization of somatostatin‐28 and somatostatin‐281–12 in monkey prefrontal cortex , 1986, The Journal of comparative neurology.

[11]  W. Nauta,et al.  Efferent connections of the substantia nigra and ventral tegmental area in the rat , 1979, Brain Research.

[12]  J. Altman,et al.  Development of the endopiriform nucleus and the claustrum in the rat brain , 1991, Neuroscience.

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

[14]  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.

[15]  J. Altman,et al.  Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. , 1993, Neurotoxicology.

[16]  T. J. Teyler,et al.  Functional relations of the rodent claustral-entorhinal-hippocampal system , 1986, Brain Research.

[17]  R. Post,et al.  Specific amygdaloid nuclei are involved in suppression or propagation of epileptiform activity during transition stage between oral automatisms and generalized clonic seizures , 2000, Brain Research.

[18]  P. Luiten,et al.  Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus , 1987, The Journal of comparative neurology.

[19]  H. Kita,et al.  Amygdaloid projections to the frontal cortex and the striatum in the rat , 1990, The Journal of comparative neurology.

[20]  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.

[21]  A. Parent,et al.  Axonal arborization of corticostriatal and corticothalamic fibers arising from prelimbic cortex in the rat. , 1998, Cerebral cortex.

[22]  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.

[23]  M. E. Corcoran,et al.  Susceptibility to Kindling and Neuronal Connections of the Anterior Claustrum , 2001, The Journal of Neuroscience.

[24]  Joseph E LeDoux.  Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[25]  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.

[26]  Joseph E LeDoux,et al.  Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala , 1997, Trends in Neurosciences.

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

[28]  M. Molinari,et al.  The organization of the ipsi- and contralateral claustrocortical system in rat with notes on the bilateral claustrocortical projections in cat , 1985, Neuroscience.

[29]  Sheng Chen,et al.  Parvalbumin and calbindin in the rat claustrum: An immunocytochemical study combined with retrograde tracing from frontoparietal cortex , 1993, Journal of Chemical Neuroanatomy.

[30]  H. Wiśniewski,et al.  The limbic zone of the rabbit and rat claustrum: a study of the claustrocingulate connections based on the retrograde axonal transport of fluorescent tracers , 2000, Anatomy and Embryology.

[31]  Kindling antagonism: interactions of the amygdala with the piriform, perirhinal, and insular cortices , 1996, Brain Research.

[32]  M. Sarter,et al.  Convergence of basolateral amygdaloid and mediodorsal thalamic projections in different areas of the frontal cortex in the rat , 1983, Brain Research Bulletin.

[33]  J. Wada,et al.  Claustrum and Amygdaloid Kindling , 1990 .

[34]  Joseph E LeDoux,et al.  Intrinsic connections of the rat amygdaloid complex: Projections originating in the basal nucleus , 1995, The Journal of comparative neurology.

[35]  Asla Pitkänen,et al.  Amygdala damage in experimental and human temporal lobe epilepsy , 1998, Epilepsy Research.

[36]  C. Frederickson,et al.  Zinc‐containing afferent projections to the rat corticomedial amygdaloid complex: A retrograde tracing study , 1998, The Journal of comparative neurology.

[37]  R. Druga.  Efferent projections from the claustrum (an experimental study using Nauta's method). , 1972, Folia morphologica.

[38]  J. Stevens,et al.  γ‐Vinyl GABA in Endopiriform Area Suppresses Kindled Amygdala Seizures , 1988 .

[39]  T. Hattori,et al.  Topographic organization and collateralization of claustrocortical projections in the rat , 1986, Brain Research Bulletin.

[40]  Joseph E LeDoux,et al.  Intrinsic connections of the rat amygdaloid complex: Projections originating in the accessory basal nucleus , 1996, The Journal of comparative neurology.

[41]  M. P. Witter,et al.  Reciprocal connections of the insular and piriform claustrum with limbic cortex: An anatomical study in the cat , 1988, Neuroscience.

[42]  L W Swanson,et al.  Connections of the posterior nucleus of the amygdala , 1992, The Journal of comparative neurology.

[43]  J. Wada,et al.  Effect of unilateral claustral lesion on intermittent light stimulation-induced convulsive response in D,L-allylglycine treated cats. , 1995, Electroencephalography and clinical neurophysiology.

[44]  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.

[45]  L. Haberly,et al.  Intrinsic and efferent connections of the endopiriform nucleus in rat , 1999, The Journal of comparative neurology.

[46]  J. Stevens,et al.  Gamma-vinyl-GABA in endopiriform area suppresses kindled amygdala seizures , 1989, Neurophysiologie clinique.

[47]  M. Zirlinger,et al.  Amygdala-enriched genes identified by microarray technology are restricted to specific amygdaloid subnuclei , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  K. Usunoff,et al.  Retrograde transport of fluorescent tracers reveals extensive ipsi‐ and contralateral claustrocortical connections in the rat , 1986, The Journal of comparative neurology.

[49]  A. Peters,et al.  Sensory-Motor Areas and Aspects of Cortical Connectivity , 1986, Cerebral Cortex.

[50]  M. Lipowska,et al.  The connections of the endopiriform nucleus with the insular claustrum in the rat and rabbit. , 2000, Folia morphologica.

[51]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[52]  J. Wada,et al.  Involvement of the claustrum in the convulsive evolution of temporal limbic seizure in feline amygdaloid kindling. , 1997, Electroencephalography and clinical neurophysiology.

[53]  G. Paxinos.  The Rat nervous system , 1985 .

[54]  P. Gloor,et al.  Role of the amygdala in temporal lobe epilepsy. , 1992 .

[55]  M. Lehman,et al.  Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual behavior: Autoradiographic and behavioral analyses , 1982, Brain Research.

[56]  S. Kuroda,et al.  A behavioral and immunohistochemical study on the development of perirhinal cortical kindling: a comparison with other types of limbic kindling , 1998, Brain Research.

[57]  M. Witter,et al.  Afferents to the seizure-sensitive neurons in layer III of the medial entorhinal area: a tracing study in the rat , 1996, Experimental Brain Research.

[58]  J. Dziewia̧tkowski,et al.  Comparative Anatomy of the Claustrum in Selected Species: A Morphometric Analysis , 1998, Brain, Behavior and Evolution.

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

[60]  M. Sadowski,et al.  Rat's claustrum shows two main cortico-related zones , 1997, Brain Research.

[61]  M. Kliot,et al.  Hippocampal afterdischarges: differential spread of activity shown by the [14C]deoxyglucose technique. , 1979, Science.

[62]  R. Reep,et al.  Neuronal connections of orbital cortex in rats: topography of cortical and thalamic afferents , 1996, Experimental Brain Research.

[63]  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.

[64]  Helen Sherk,et al.  The Claustrum and the Cerebral Cortex , 1986 .

[65]  T. L. Neal,et al.  The rat claustrum: Afferent and efferent connections with visual cortex , 1985, Brain Research.

[66]  H. Groenewegen,et al.  Connections of the parahippocampal cortex in the cat. II. Subcortical afferents , 1986, The Journal of comparative neurology.

[67]  M. E. Corcoran,et al.  Kindling of claustrum and insular cortex: comparison to perirhinal cortex in the rat , 2001, The European journal of neuroscience.

[68]  R. Druga.  Claustro-neocortical connections in the cat and rat demonstrated by HRP tracing technique. , 1982, Journal fur Hirnforschung.

[69]  J. Price,et al.  Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat , 1977, The Journal of comparative neurology.

[70]  M. E. Corcoran,et al.  Claustral Lesions Delay Amygdaloid Kindling in the Rat , 2000, Epilepsia.

[71]  W. Cowan,et al.  A study of subcortical afferents to the hippocampal formation in the rat , 1979, Neuroscience.

[72]  R. Druga,et al.  Claustro-neocortical projections in the rhesus monkey (projections to area 6). , 1990, Journal fur Hirnforschung.

[73]  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.

[74]  H. Groenewegen,et al.  Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat , 1996, Neuroscience.

[75]  G. Schoenbaum,et al.  Functions of the Amygdala and Related Forebrain Areas in Attention and Cognition , 1999, Annals of the New York Academy of Sciences.

[76]  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 .