Zinc‐containing afferent projections to the rat corticomedial amygdaloid complex: A retrograde tracing study

The mammalian amygdaloid complex is densely innervated by zinc‐containing neurons. The distribution of the terminals throughout the region has been described, but the origins of these zinc‐containing fibers have not. The present work describes the origins of one major component of the zinc‐containing innervation of the amygdaloid complex, namely, the component that innervates the corticomedial complex. Selective labeling of zinc‐containing axons was accomplished by intracerebral microinfusion of selenium anions (SeO32−), a procedure that produces a ZnSe precipitate in zinc‐containing axonal boutons with subsequent retrograde transport to the neurons of origin. After infusions of SeO32− into combinations of cortical, medial, or amygdalohippocampal regions, retrogradely labeled zinc‐containing somata were found in all amygdaloid nuclei except for the medial and central nuclei, the bed nucleus of the accessory olfactory tract, the nucleus of the lateral olfactory tract, and the anterior amygdaloid area. Extrinsic zinc‐containing projections to the same amygdaloid terminal fields were found to originate from the infralimbic, cingulate, piriform, perirhinal and entorhinal cortices, and from the prosubiculum and CA1. Commissural zinc‐containing projections were found to originate from the posterolateral and posteromedial cortical nuclei and from the posterior part of the basomedial nucleus. Zinc‐containing neurons have been implicated in the pathophysiology of epilepsy, in cell death after seizure or stroke, and in Alzheimer's disease, all clinical conditions that involve the amygdaloid complex. Identification of the zinc‐containing pathways is a prerequisite to the elucidation of zinc's role in these disorders. J. Comp. Neurol. 400:375–390, 1998. © 1998 Wiley‐Liss, Inc.

[1]  S. Jackson,et al.  The selection and suppression of action: ERP correlates of executive control in humans. , 1999, Neuroreport.

[2]  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.

[3]  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.

[4]  A. Connelly,et al.  The amygdala and intractable temporal lobe epilepsy , 1996, Neurology.

[5]  J. Gotman,et al.  Amygdala-hippocampus relationships in temporal lobe seizures: a phase-coherence study , 1996, Epilepsy Research.

[6]  J. Pérez‐clausell Distribution of terminal fields stained for zinc in the neocortex of the rat , 1996, Journal of Chemical Neuroanatomy.

[7]  J. Gotman,et al.  Significance of mesial temporal atrophy in relation to intracranial ictal and interictal stereo EEG abnormalities. , 1996, Brain : a journal of neurology.

[8]  H. Soininen,et al.  SPECT and MRI analysis in Alzheimer's disease: relation to apolipoprotein E epsilon 4 allele. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[9]  Yong Y. He,et al.  The Role of Zinc in Selective Neuronal Death After Transient Global Cerebral Ischemia , 1996, Science.

[10]  Joseph E LeDoux,et al.  Emotion: Systems, Cells, Synaptic Plasticity , 1996, Cell.

[11]  R. Kuzniecky,et al.  Qualitative MRI Segmentation in Mesial Temporal Sclerosis: Clinical Correlations , 1996, Epilepsia.

[12]  A. McDonald,et al.  Glutamate and aspartate immunoreactive neurons of the rat basolateral amygdala: Colocalization of excitatory amino acids and projections to the limbic circuit , 1996, The Journal of comparative neurology.

[13]  P. Mantyh,et al.  Zinc‐Induced Aggregation of Human and Rat β‐Amyloid Peptides In Vitro , 1996 .

[14]  F. Boller,et al.  Specificity of temporal amygdala atrophy in Alzheimer's disease: quantitative assessment with magnetic resonance imaging. , 1996, Dementia.

[15]  A. Williamson,et al.  Zinc reduces dentate granule cell hyperexcitability in epileptic humans , 1995, Neuroreport.

[16]  Christopher J. Frederickson,et al.  Zinc-containing innervation of the subicular region in the rat , 1995, Neurochemistry International.

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

[18]  A. Schousboe,et al.  Citrate modulates the regulation by Zn2+ of N-methyl-D-aspartate receptor-mediated channel current and neurotransmitter release. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[19]  F. Martínez-García,et al.  Callosal neurones give rise to zinc-rich boutons in the rat visual cortex. , 1995, Neuroreport.

[20]  H. Barbas,et al.  Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey , 1995, Hippocampus.

[21]  C. Frederickson,et al.  A zinc‐containing fiber system of thalamic origin , 1994, Neuroreport.

[22]  D. Moncrieff,et al.  Zinc-containing neurons. , 1994, Biological signals.

[23]  D. Paré,et al.  Intra‐amygdaloid projections of the lateral nucleus in the cat: PHA‐L anterograde labeling combined with postembedding GABA and glutamate immunocytochemistry , 1994, The Journal of comparative neurology.

[24]  T. Smart,et al.  Modulation of inhibitory and excitatory amino acid receptor ion channels by zinc , 1994, Progress in Neurobiology.

[25]  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.

[26]  Huaying Xu,et al.  Chelation of zinc by diethyldithiocarbamate facilitates bursting induced by mixed antidromic plus orthodromic activation of mossy fibers in hippocampal slices , 1993, Brain Research.

[27]  C. Masters,et al.  A novel zinc(II) binding site modulates the function of the beta A4 amyloid protein precursor of Alzheimer's disease. , 1993, The Journal of biological chemistry.

[28]  C. Mitchell,et al.  Proconvulsant action of diethyldithiocarbamate in stimulation of the perforant path. , 1993, Neurotoxicology and teratology.

[29]  G. A. Howell,et al.  Zinc-containing neuronal innervation of the septal nuclei , 1993, Brain Research.

[30]  S. Nakanishi,et al.  Molecular cloning and chromosomal localization of the key subunit of the human N-methyl-D-aspartate receptor. , 1993, The Journal of biological chemistry.

[31]  G. A. Howell,et al.  Distribution of histochemically reactive zinc in the forebrain of the rat , 1992, Journal of Chemical Neuroanatomy.

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

[33]  M. Cynader,et al.  Enrichment of glutamate in zinc-containing terminals of the cat visual cortex. , 1992, Neuroreport.

[34]  Robert H. Perry,et al.  [3H]MK-801 binding to the NMDA receptor complex, and its modulation in human frontal cortex during development and aging , 1992, Brain Research.

[35]  G. Danscher,et al.  Retrograde tracing of zinc-containing neurons by selenide ions: a survey of seven selenium compounds. , 1992, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[36]  J. Han,et al.  Serotonergic projections from the nucleus raphe dorsalis to the amygdala in the rat , 1991, Neuroscience Letters.

[37]  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.

[38]  G. A. Howell,et al.  Zinc containing projections to the bed nucleus of the stria terminalis , 1991, Brain Research.

[39]  S. Evans,et al.  Presence of a cholinergic projection from ventral striatum to amygdala that is not immunoreactive for NGF receptor , 1991, Neuroscience Letters.

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

[41]  G. Danscher,et al.  Labeling of the neurons of origin of zinc-containing pathways by intraperitoneal injections of sodium selenite , 1990, Neuroscience.

[42]  G. A. Howell,et al.  A retrograde transport method for mapping zinc-containing fiber systems in the brain , 1990, Brain Research.

[43]  G. A. Howell,et al.  Effects of Subcutaneous Injections of Zinc Chloride on Seizures Induced by Noise and by Kainic Acid , 1990, Epilepsia.

[44]  A. Constanti,et al.  Differential effect of zinc on the vertebrate GABAA‐receptor complex , 1990, British journal of pharmacology.

[45]  J. Zimmer,et al.  Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat , 1990, Neuroscience Letters.

[46]  D. Choi,et al.  Effect of zinc on NMDA receptor-mediated channel currents in cortical neurons , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  C. Köhler,et al.  Subicular projections to the hypothalamus and brainstem: some novel aspects revealed in the rat by the anterograde Phaseolus vulgaris leukoagglutinin (PHA-L) tracing method. , 1990, Progress in brain research.

[48]  G. Danscher,et al.  Amygdaloid efferents through the stria terminalis in the rat give origin to zinc‐containing boutons , 1989, The Journal of comparative neurology.

[49]  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.

[50]  J. McGinty,et al.  Translocation of zinc may contribute to seizure-induced death of neurons , 1989, Brain Research.

[51]  C. Frederickson Neurobiology of zinc and zinc-containing neurons. , 1989, International review of neurobiology.

[52]  G. A. Howell,et al.  Zinc-containing fiber systems in the cochlear nuclei of the rat and mouse , 1988, Hearing Research.

[53]  D. Choi,et al.  Zinc alters excitatory amino acid neurotoxicity on cortical neurons , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  J. McGinty,et al.  Loss of zinc staining from hippocampal mossy fibers during kainic acid induced seizures: a histofluorescence study , 1988, Brain Research.

[55]  C. Frederickson Hippocampal Zinc, The Storage Granule Pool: Localization, Physiochemistry, and Possible Functions , 1988 .

[56]  M. J. Christie,et al.  Excitatory amino acid projections to the nucleus accumbens septi in the rat: A retrograde transport study utilizingd[3H]aspartate and [3H]GABA , 1987, Neuroscience.

[57]  M. Mayer,et al.  Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons , 1987, Nature.

[58]  D. Choi,et al.  Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. , 1987, Science.

[59]  Y. Ben-Ari,et al.  Selective release of endogenous zinc from the hippocampal mossy fibers in situ , 1987, Brain Research.

[60]  Douglas L. Rosene,et al.  The Hippocampal Formation of the Primate Brain , 1987 .

[61]  L. Swanson,et al.  Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  M. Sakanaka,et al.  Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex , 1986, Brain Research.

[63]  M. Cassell,et al.  Topography of projections from the medial prefrontal cortex to the amygdala in the rat , 1986, Brain Research Bulletin.

[64]  J. Price,et al.  The distribution of choline acetyltransferase in the rat amygdaloid complex and adjacent cortical areas, as determined by quantitative micro‐assay and immunohistochemistry , 1986, The Journal of comparative neurology.

[65]  J. Storm-Mathisen,et al.  Putative amino acid transmitters in the amygdala. , 1986, Advances in experimental medicine and biology.

[66]  I. Crawford Relationship of glutamic acid and zinc to kindling of the rat amygdala: afferent transmitter systems and excitability in a model of epilepsy. , 1986, Advances in experimental medicine and biology.

[67]  L. Heimer,et al.  Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: A combined retrograde fluorescent and immunohistochemical study , 1985, The Journal of comparative neurology.

[68]  R. S. Sloviter A selective loss of hippocampal mossy fiber Timm stain accompanies granule cell seizure activity induced by perforant path stimulation , 1985, Brain Research.

[69]  T. Chiba,et al.  Afferent and efferent connections of the medial preoptic area in the rat: A WGA-HRP study , 1985, Brain Research Bulletin.

[70]  J. Zimmer,et al.  The architecture and some of the interconnections of the rat's amygdala and lateral periallocortex , 1984, The Journal of comparative neurology.

[71]  G. A. Howell,et al.  Stimulation-induced uptake and release of zinc in hippocampal slices , 1984, Nature.

[72]  Shin-Ho Chung,et al.  Release of endogenous Zn2+ from brain tissue during activity , 1984, Nature.

[73]  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.

[74]  F. Fonnum,et al.  Regional cortical glutamergic and aspartergic projections to the amygdala and thalamus of the rat , 1983, Brain Research.

[75]  L. Butcher,et al.  Cholinergic projections to the basolateral amygdala: A combined Evans Blue and acetylcholinesterase analysis , 1982, Brain Research Bulletin.

[76]  T. Maeda,et al.  Cholinergic projections from the basal forebrain of rat to the amygdala , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  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.

[78]  L. Nitecka,et al.  Interamygdaloid connections in the rat studied by the horseradish peroxidase method , 1981, Neuroscience Letters.

[79]  J M Wyss,et al.  An autoradiographic study of the efferent connections of the entorhinal cortex in the rat , 1981, The Journal of comparative neurology.

[80]  H. Steinbusch,et al.  Distribution of serotonin-immunoreactivity in the central nervous system of the rat—Cell bodies and terminals , 1981, Neuroscience.

[81]  S. Bayer,et al.  Quantitative 3H‐thymidine radiographic analyses of neurogenesis on the rat amygdala , 1980, The Journal of comparative neurology.

[82]  O. Ottersen Afferent connections to the amygdaloid complex of the rat and cat: II. Afferents from the hypothalamus and the basal telencephalon , 1980, The Journal of comparative neurology.

[83]  J. P. Flynn,et al.  Afferent projections to affective attack sites in cat hypothalamus , 1980, Brain Research.

[84]  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.

[85]  Y. Ben-Ari,et al.  Choline acetyltransferase and acetylcholinesterase containing projections from the basal forebrain to the amygdaloid complex of the rat , 1979, Brain Research.

[86]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain II. Amygdala, suprarhinal cortex and entorhinal cortex , 1978, The Journal of comparative neurology.

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

[88]  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.

[89]  B. K. Hartman,et al.  The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine‐B‐hydroxylase as a marker , 1975, The Journal of comparative neurology.

[90]  Smejda Haug Fm Heavy metals in the brain. A light microscope study of the rat with Timm's sulphide silver method. Methodological considerations and cytological and regional staining patterns. , 1973 .

[91]  J. D. Olmos,et al.  The Amygdaloid Projection Field in the Rat as Studied with the Cupric-Silver Method , 1972 .