Chapter VII Chemical neuroanatomy of the primate insula cortex: Relationship to cytoarchitectonics, connectivity, function and neurodegeneration

Publisher Summary This chapter discusses the chemoanatomy of the primate insula and reviews the alterations in the neurotransmitter systems within the insula during aging and neurodegenerative disease. The primate insula is situated on the surface of the cerebral hemisphere early in embryogenesis. Adjacent neocortical areas develop much more extensively than the insula during fetal development. This extensive cortical maturation leads to massive frontal, parietal, and temporal opercularization and to the formation of the Sylvian fissure. The insula remains buried within the Sylvian fissure from birth onwards. In subprimates, the neocortex does not develop extensively. Therefore, the homologue of the primate insula remains exposed on the cortical surface during the life of the organism. Despite its covered location deep within the Sylvian fissure that prevents direct visualization, awareness of the insula has existed for over four hundred years.

[1]  M. Mesulam,et al.  Cortical effects of neurotoxic damage to the nucleus basalis in rats: persistent loss of extrinsic cholinergic input and lack of transsynaptic effect upon the number of somatostatin-containing, cholinesterase-positive, and cholinergic cortical neurons , 1987, Brain Research.

[2]  D. Price,et al.  Evidence for cholinergic neurites in senile plaques. , 1984, Science.

[3]  P. Davies,et al.  Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. , 1992, The Journal of biological chemistry.

[4]  Joseph B. Martin,et al.  Somatostatin is increased in the nucleus accumbens in Huntington's disease , 1984, Neurology.

[5]  E. Mufson,et al.  NGF receptor (p75)‐immunoreactivity in the developing primate basal ganglia , 1993, The Journal of comparative neurology.

[6]  L. Hersh,et al.  Neurofibrillary tangles in cholinergic pedunculopontine neurons in Alzheimer's disease , 1988, Annals of neurology.

[7]  M. Mishkin,et al.  Projections from behaviorally-defined sectors of the prefrontal cortex to the basal ganglia, septum, and diencephalon of the monkey. , 1968, Experimental neurology.

[8]  J. DeFelipe,et al.  Parvalbumin immunoreactivity reveals layer IV of monkey cerebral cortex as a mosaic of microzones of thalamic afferent terminations , 1991, Brain Research.

[9]  E. Mufson,et al.  Reduced nicotinamide adenine dinucleotide phosphate‐diaphorase/nitric oxide synthase profiles in the human hippocampal formation and perirhinal cortex , 1995, The Journal of comparative neurology.

[10]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[11]  R. Weinberg,et al.  Neurons in rat hippocampus that synthesize nitric oxide , 1993, The Journal of comparative neurology.

[12]  R. Katzman.,et al.  Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa , 1980, Nature.

[13]  Z. Khachaturian.  Diagnosis of Alzheimer's disease. , 1985, Archives of neurology.

[14]  C. Geula,et al.  Anatomy of cholinesterase inhibition in Alzheimer's disease: Effect of physostigmine and tetrahydroaminoacridine on plaques and tangles , 1987, Annals of neurology.

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

[16]  E. Mufson,et al.  Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseased brain , 1997, Neuroscience.

[17]  P. Gloor,et al.  The role of the limbic system in experiential phenomena of temporal lobe epilepsy , 1982, Annals of neurology.

[18]  N. Ling,et al.  Hypothalamic Polypeptide That Inhibits the Secretion of Immunoreactive Pituitary Growth Hormone , 1973, Science.

[19]  L. Hersh,et al.  Nerve growth factor receptor immunoreactive profiles in the normal, aged human basal forebrain: Colocalization with cholinergic neurons , 1989, The Journal of comparative neurology.

[20]  H. Kimura,et al.  Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry , 1983, Journal of Neuroscience Methods.

[21]  A. Peters,et al.  Somatostatin immunoreactive neurons in rat visual cortex: A light and electron microscopic study , 1986, Journal of neurocytology.

[22]  J. Garthwaite,et al.  Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain , 1988, Nature.

[23]  F. D. Silva,et al.  Kindling induced changes in parvalbumin immunoreactivity in rat hippocampus and its relation to long-term decrease in GABA-immunoreactivity , 1989, Brain Research.

[24]  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.

[25]  H. Harlow,et al.  The History and Philosophy of Knowledge of the Brain and its Functions , 1960, Neurology.

[26]  E. Mufson,et al.  Galanin‐like immunoreactivity within the primate basal forebrain: Differential staining patterns between humans and monkeys , 1990, The Journal of comparative neurology.

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

[28]  M. Celio,et al.  Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. , 1986, Science.

[29]  P. Rakić,et al.  Multiple types of neuropeptide Y‐containing neurons in primate neocortex , 1989, The Journal of comparative neurology.

[30]  B. Whitsel,et al.  Patterns of metabolic activity in cytoarchitectural area SII and surrounding cortical fields of the monkey. , 1983, Journal of neurophysiology.

[31]  M. Mesulam,et al.  Neural inputs into the temporopolar cortex of the rhesus monkey , 1987, The Journal of comparative neurology.

[32]  D. Price,et al.  Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  W. Benzing,et al.  Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging, Alzheimer's disease and Down's syndrome. , 1993, Dementia.

[34]  F. P. Wirth.  Insular‐diencephalic connections in the Macaque , 1973, The Journal of comparative neurology.

[35]  B. Berger,et al.  Subpopulations of somatostatin 28-immunoreactive neurons display different vulnerability in senile dementia of the Alzheimer type , 1989, Brain Research.

[36]  S H Snyder,et al.  A novel neuronal messenger molecule in brain: The free radical, nitric oxide , 1992, Annals of neurology.

[37]  P. Hof,et al.  Regional distribution of neurofilament and calcium-binding proteins in the cingulate cortex of the macaque monkey. , 1992, Cerebral cortex.

[38]  M. Mesulam,et al.  Immunohistochemical evidence for a possible somatostatin-containing amygdalostriatal pathway in normal and Alzheimer's disease brain , 1988, Brain Research.

[39]  D. McCormick,et al.  Two types of muscarinic response to acetylcholine in mammalian cortical neurons. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[41]  V. Mutt,et al.  Neuropeptide Y—a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide , 1982, Nature.

[42]  M. Mesulam,et al.  Regional variations in cortical cholinergic innervation: Chemoarchitectonics of acetylcholinesterase-containing fibers in the macaque brain , 1984, Brain Research.

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

[44]  H. Bittiger,et al.  Central actions of somatostatin. , 1980, European journal of pharmacology.

[45]  C Yamamoto,et al.  Presynaptic action of acetylcholine in thin sections from the guinea pig dentate gyrus in vitro. , 1967, Experimental neurology.

[46]  Margaret A. Pericak-Vance,et al.  Hypothesis: Microtubule Instability and Paired Helical Filament Formation in the Alzheimer Disease Brain Are Related to Apolipoprotein E Genotype , 1994, Experimental Neurology.

[47]  K. Pribram,et al.  Neuronographic analysis of medial and basal cerebral cortex. II. Monkey. , 1953, Journal of neurophysiology.

[48]  F. Bloom,et al.  Evidence for selective release of somatostatin-14 and somatostatin-28(1- 12) from rat hypothalamus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  H. Kuypers,et al.  Cells of origin of cortical projections to dorsal column nuclei, spinal cord and bulbar medial reticular formation in the rhesus monkey , 1976, Neuroscience Letters.

[50]  R. S. Sloviter.  Calcium‐binding protein (calbindin‐D28k) and parvalbumin immunocytochemistry: Localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity , 1989, The Journal of comparative neurology.

[51]  M. Molinari,et al.  Auditory thalamocortical pathways defined in monkeys by calcium‐binding protein immunoreactivity , 1995, The Journal of comparative neurology.

[52]  R. Mahley,et al.  Conformation of apolipoprotein E in lipoproteins. , 1993, The Journal of biological chemistry.

[53]  D. Pandya,et al.  Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey. , 1971, Brain research.

[54]  M. Pericak-Vance,et al.  Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[55]  R. Mahley,et al.  Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. , 1988, Science.

[56]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[57]  S. Tanaka,et al.  Stimulatory effect of somatostatin on norepinephrine release from rat brain cortex slices. , 1981, Life sciences.

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

[59]  J. Coyle,et al.  Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. , 1982, Science.

[60]  J. R. Augustine,et al.  Immunocytochemical staining of neuropeptide Y (NPY) in the insular lobe of the monkey: a light microscopic study , 1993, Brain Research.

[61]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[62]  B. Wainer,et al.  Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat , 1988, The Journal of comparative neurology.

[63]  E. Mufson,et al.  Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: A quantitative analysis across subregions of the basal forebrain , 1989, Experimental Neurology.

[64]  M M Mesulam,et al.  Systematic regional differences in the cholinergic innervation of the primate cerebral cortex: Distribution of enzyme activities and some behavioral implications , 1986, Annals of neurology.

[65]  D. Amaral,et al.  Distribution of reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPH‐d) cells and fibers in the monkey amygdaloid complex , 1991, The Journal of comparative neurology.

[66]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[67]  Joseph B. Martin,et al.  Somatostatin-281–12-like immunoreactivity is reduced in Alzheimer's disease cerebral cortex , 1986, Brain Research.

[68]  E. Mufson,et al.  Reduced nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) profiles in the amygdala of human and new world monkey (Saimiri sciureus) , 1992, Brain Research.

[69]  K. Pribram,et al.  Cortical organization in gustation (Macaca mulatta). , 1953, Journal of neurophysiology.

[70]  E. Mufson,et al.  Reduced nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry in the hippocampal formation of the new world monkey (Saimiri sciureus) , 1990, Brain Research.

[71]  D. Pandya,et al.  Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey. , 1971, Brain research.

[72]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

[73]  M M Mesulam,et al.  Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus , 1984, The Journal of comparative neurology.

[74]  E. Mufson,et al.  Galanin immunoreactivity in the primate central nervous system , 1992, The Journal of comparative neurology.

[75]  J. Taylor,et al.  Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. , 1985, The Journal of clinical investigation.

[76]  H. Burton,et al.  Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis , 1980, The Journal of comparative neurology.

[77]  R. S. Sloviter,et al.  Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: The “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy , 1991, Hippocampus.

[78]  A. Levey,et al.  The origins of cholinergic and other subcortical afferents to the thalamus in the rat , 1987, The Journal of comparative neurology.

[79]  W. Benzing,et al.  Apolipoprotein E immunoreactivity within neurofibrillary tangles: relationship to tau and PHF in Alzheimer's disease , 1995, Experimental Neurology.

[80]  J. Kordower,et al.  Nerve growth factor receptor immunoreactivity in the nonhuman primate (Cebus apella): Distribution, morphology, and colocalization with cholinergic enzymes , 1988, The Journal of comparative neurology.

[81]  M. Mesulam,et al.  The Insula of Reil in Man and Monkey , 1985 .

[82]  A. Levey,et al.  Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  J. Morrison,et al.  Human orbitofrontal cortex: Cytoarchitecture and quantitative immunohistochemical parcellation , 1995, The Journal of comparative neurology.

[84]  W. Benzing,et al.  Galanin immunoreactivity within the primate basal forebrain: Evolutionary change between monkeys and apes , 1993, The Journal of comparative neurology.

[85]  D. Amaral,et al.  The distribution of somatostatin‐like immunoreactivity in the monkey hippocampal formation , 1985, The Journal of comparative neurology.

[86]  W. Benzing,et al.  Increased number of NADPH-d-positive neurons within the substantia innominata in Alzheimer's disease , 1995, Brain Research.

[87]  Joseph B. Martin,et al.  Depressant action of TRH, LH-RH and somatostatin on activity of central neurones , 1975, Nature.

[88]  D. Mash,et al.  Loss of M2 muscarine receptors in the cerebral cortex in Alzheimer's disease and experimental cholinergic denervation. , 1985, Science.

[89]  S. Snyder,et al.  Relative sparing of nitric oxide synthase–containing neurons in the hippocampal formation in Alzheimer's disease , 1992, Annals of neurology.

[90]  M. Pericak-Vance,et al.  Apolipoprotein E Is Present in Hippocampal Neurons without Neurofibrillary Tangles in Alzheimer's Disease and in Age-Matched Controls , 1994, Experimental Neurology.

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

[92]  V. Chan‐Palay.  Galanin hyperinnervates surviving neurons of the human basal nucleus of meynert in dementias of alzheimer's and parkinson's disease: A hypothesis for the role of galanin in accentuating cholinergic dysfunction in dementia , 1988, The Journal of comparative neurology.

[93]  P. Klivényi,et al.  Somatostatin and Alzheimer's disease. , 1995, Archives of gerontology and geriatrics.

[94]  F. Bloom,et al.  Immunohistochemical distribution of pro-somatostatin-related peptides in cerebral cortex , 1983, Brain Research.

[95]  J. Morrison,et al.  Apolipoprotein E-immunoreactivity in aged rhesus monkey cortex: Colocalization with amyloid plaques , 1994, Neurobiology of Aging.

[96]  M M Mesulam,et al.  Distribution of muscarinic receptor subtypes within architectonic subregions of the primate cerebral cortex , 1988, The Journal of comparative neurology.

[97]  S. Snyder,et al.  Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[98]  D. Pandya,et al.  The topographical distribution of interhemispheric projections in the corpus callosum of the rhesus monkey. , 1971, Brain research.

[99]  J. Morrison,et al.  Quantitative morphology and regional and laminar distributions of senile plaques in Alzheimer's disease , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[100]  L. Iversen,et al.  Reduced amounts of immunoreactive somatostatin in the temporal cortex in senile dementia of Alzheimer type , 1980, Neuroscience Letters.

[101]  W. Staines,et al.  A galanin-like peptide coexists in putative cholinergic somata of the septum-basal forebrain complex and in acetylcholinesterase-containing fibers and varicosities within the hippocampus in the owl monkey (aotus trivirgatus) , 1986, Neuroscience Letters.

[102]  A. Levey,et al.  Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey , 1983, The Journal of comparative neurology.

[103]  T. Hökfelt,et al.  NADPH‐diaphorase: A selective histochemical marker for striatal neurons containing both somatostatin‐ and avian pancreatic polypeptide (APP)‐like immunoreactivities , 1983, The Journal of comparative neurology.

[104]  P. Emson,et al.  Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[105]  J. Morrison,et al.  Somatostatin-28 [1-12]-like peptides. , 1985, Advances in experimental medicine and biology.

[106]  K. V. Sørensen.  Somatostatin: Localization and distribution in the cortex and the subcortical white matter of human brain , 1982, Neuroscience.

[107]  F. Sanides.  The architecture of the cortical taste nerve areas in squirrel monkey (Saimiri sciureus) and their relationships to insular, sensorimotor and prefrontal regions. , 1968, Brain research.

[108]  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.

[109]  B. Bogerts,et al.  The distribution of nitric oxide synthase immunoreactivity in the human brain , 1994, Neuroscience.

[110]  T. Hashikawa,et al.  Nitric oxide synthase immunoreactivity colocalized with NADPH-diaphorase histochemistry in monkey cerebral cortex , 1994, Brain Research.

[111]  E. Mufson,et al.  Nerve growth factor receptor‐immunoreactive neurons within the developing human cortex , 1992, The Journal of comparative neurology.

[112]  Joseph B. Martin,et al.  Somatostatin is increased in the basal ganglia in Huntington disease , 1983, Annals of neurology.

[113]  G. Orban,et al.  Immunocytochemical localization of somatostatin and cholecystokinin in the cat visual cortex , 1985, Brain Research.

[114]  R. Bartus,et al.  The cholinergic hypothesis of geriatric memory dysfunction. , 1982, Science.

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

[116]  J. Schneider,et al.  Regional Variation in the Distribution of Apolipoprotein E and Aβ in Alzheimer's Disease , 1995 .

[117]  A. Solodkin,et al.  Cellular and Systems Neuroanatomical Changes in Alzheimer's Disease , 1994 .

[118]  S. Reichlin,et al.  Somatostatin in hypothalamus, extrahypothalamic brain, and peripheral tissues of the rat. , 1978, Endocrinology.

[119]  J. Allman,et al.  Organization of the face representation in macaque motor cortex , 1980, The Journal of comparative neurology.

[120]  P. Rakić,et al.  Distribution of neuropeptide y‐containing perikarya and axons in various neocortical areas in the macaque monkey , 1989, The Journal of comparative neurology.

[121]  M M Mesulam,et al.  Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. , 1984, Brain : a journal of neurology.

[122]  K. Pribram,et al.  SOME CONNECTIONS OF THE ORBITO-FRONTO-TEMPORAL, LIMBIC AND HIPPOCAMPAL AREAS OF MACACA MULATTA , 1950 .

[123]  T. Bonner,et al.  Identification of a family of muscarinic acetylcholine receptor genes. , 1987, Science.

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

[125]  Tracy Earl Clark,et al.  The comprative anatomy of the insula , 1896 .

[126]  Joseph B. Martin,et al.  Subset of neurons characterized by the presence of NADPH‐diaphorase in human substantia innominata , 1987, The Journal of comparative neurology.

[127]  E. Crosby,et al.  Correlative Anatomy of the Nervous System , 1962 .

[128]  L. Hersh,et al.  Cholinergic innervation in the human hippocampal formation including the entorhinal cortex , 1994, The Journal of comparative neurology.

[129]  S. Vincent,et al.  Somatostatin- and Neuropeptide Y-immunoreactive neurons in the neocortex in senile dementia of alzheimer's type , 1986, Brain Research.

[130]  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.

[131]  E. Mufson,et al.  Ultrastructural localization of acetylcholinesterase in neurofibrillary tangles, neuropil threads and senile plaques in aged and Alzheimer's brain , 1992, Brain Research.

[132]  T. Rasmussen,et al.  Stimulation studies of insular cortex of Macaca mulatta. , 1953, Journal of neurophysiology.

[133]  M. J. Showers.  Correlation of medial thalamic nuclear activity with cortical and subcortical neuronal arcs , 1958, The Journal of comparative neurology.

[134]  E. W. Lauer,et al.  Somatovisceral motor patterns in the insula , 1961, The Journal of comparative neurology.

[135]  A. Brun,et al.  Regional pattern of degeneration in Alzheimer's disease: neuronal loss and histopathological grading , 1981, Histopathology.

[136]  S. L. Dun,et al.  Colocalization of nitric oxide synthase and somatostatin immunoreactivity in rat dentate hilar neurons. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[137]  W. Benzing,et al.  Evidence that transmitter‐containing dystrophic neurites precede paired helical filament and Alz‐50 formation within senile plaques in the amygdala of nondemented elderly and patients with Alzheimer's disease , 1993, The Journal of comparative neurology.

[138]  J. Lund,et al.  Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin‐releasing factor‐and parvalbumin‐immunoreactive populations , 1990, The Journal of comparative neurology.

[139]  W. Penfield,et al.  The insula; further observations on its function. , 1955, Brain : a journal of neurology.

[140]  G K Wilcock,et al.  Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[141]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[142]  A Reeves,et al.  Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey. , 1971, Brain research.

[143]  E. Mufson,et al.  Sparing of NADPH-diaphorase striatal neurons in Parkinson's and Alzheimer's diseases. , 1994, Neuroreport.

[144]  Myron S. Jacobs,et al.  The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Surface configurations of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetacean species , 1980, Brain Research Bulletin.

[145]  D. Drachman,et al.  Human memory and the cholinergic system. A relationship to aging? , 1974, Archives of neurology.

[146]  S. Vincent,et al.  Striatal neurons containing both somatostatin‐ and avian pancreatic polypeptide (APP)‐like immunoreactivities and NADPH‐diaphorase activity: A light and electron microscopic study , 1983, The Journal of comparative neurology.

[147]  John P. Robarts,et al.  Neuropeptide changes following excitotoxic lesion of the insular cortex in rats , 1995, The Journal of comparative neurology.