Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey

The sources of ipsilateral projections from the hippocampal formation, the presubiculum, area 29a‐c, and parasubiculum to medial, orbital, and lateral prefrontal cortices were studied with retrograde tracers in 27 rhesus monkeys. Labeled neurons within the hippocampal formation (CA1, CA1′, prosubiculum, and subiculum) were found rostrally, although some were noted throughout the entire rostrocaudal extent of the hippocampal formation. Most labeled neurons in the hippocampal formation projected to medial prefrontal cortices, followed by orbital areas. In addition, there were differences in the topography of afferent neurons projecting to medial when compared with orbital cortices. Labeled neurons innervating medial cortices were found mainly in the CA1′ and CA1 fields rostrally, but originated in the subicular fields caudally. In contrast, labeled neurons which innervated orbital cortices were considerably more focal, emanating from the same relative position within a field throughout the rostrocaudal extent of the hippocampal formation.

[1]  H. Barbas,et al.  Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex , 1995, Neuroscience & Biobehavioral Reviews.

[2]  P Alvarez,et al.  Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  H. Barbas.  Pattern in the cortical distribution of prefrontally directed neurons with divergent axons in the rhesus monkey. , 1995, Cerebral cortex.

[4]  H. Barbas,et al.  Contralateral thalamic projections predominantly reach transitional cortices in the rhesus monkey , 1994, The Journal of comparative neurology.

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

[6]  L. Beason-Held.  Contributions of the hippocampus and related ventromedial temporal cortices to memory in the rhesus monkey , 1994 .

[7]  A. Damasio.  Descarte's error : emotion, reason, and the human brain , 1994 .

[8]  J. Price,et al.  The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[9]  H. Barbas,et al.  Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey , 1993, Neuroscience.

[10]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[11]  J. Fuster.  Frontal lobes , 1993, Current Opinion in Neurobiology.

[12]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[13]  L. Squire,et al.  Neuroanatomy of memory. , 1993, Annual review of neuroscience.

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

[15]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[16]  Michael Davis,et al.  The role of the amygdala in fear and anxiety. , 1992, Annual review of neuroscience.

[17]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

[18]  H. Barbas,et al.  Diverse thalamic projections to the prefrontal cortex in the rhesus monkey , 1991, The Journal of comparative neurology.

[19]  L. Squire,et al.  Independence of memory functions and emotional behavior: Separate contributions of the hippocampal formation and the amygdala , 1991, Hippocampus.

[20]  P. Goldman-Rakic,et al.  D1 dopamine receptors in prefrontal cortex: involvement in working memory , 1991, Science.

[21]  M. Gershon,et al.  Evaluation of the activity of chemically identified enteric neurons through the histochemical demonstration of cytochrome oxidase , 1990, The Journal of comparative neurology.

[22]  H. Barbas,et al.  Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey , 1990, The Journal of comparative neurology.

[23]  G. Alheid.  19 – Basal Ganglia , 1990 .

[24]  David G. Amaral,et al.  21 – Hippocampal Formation , 1990 .

[25]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[26]  G. F. Tremblay,et al.  The Prefrontal Cortex , 1989, Neurology.

[27]  L. Squire,et al.  Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  A P Shimamura,et al.  Cognitive impairment following frontal lobe damage and its relevance to human amnesia. , 1989, Behavioral neuroscience.

[29]  L R Squire,et al.  Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[31]  K Watanabe,et al.  Connections of area 8 with area 6 in the brain of the macaque monkey , 1988, The Journal of comparative neurology.

[32]  M. Mishkin,et al.  A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  H. Barbas.  Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[34]  H Nishijo,et al.  Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Kisou Kubota,et al.  Dopamine enhances the neuronal activity of spatial short-term memory task in the primate prefrontal cortex , 1988, Neuroscience Research.

[36]  D L Rosene,et al.  A comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: I. Convergence in the entorhinal, prorhinal, and perirhinal cortices , 1988, The Journal of comparative neurology.

[37]  P. Goldman-Rakic.  Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[38]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[39]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

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

[41]  H. Barbas.  Pattern in the laminar origin of corticocortical connections , 1986, The Journal of comparative neurology.

[42]  D. Rosene,et al.  A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. , 1986, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[43]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[45]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[46]  M. Voytko.  Cooling orbital frontal cortex disrupts matching-to-sample and visual discrimination learning in monkeys , 1985 .

[47]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[48]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.

[49]  D. Benson,et al.  Amnesia with hippocampal lesions after cardiopulmonary arrest. , 1996, Neurology.

[50]  Michael Petrides,et al.  Behavioural effects of frontal-lobe lesions in man , 1984, Trends in Neurosciences.

[51]  P. Goldman-Rakic,et al.  Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey , 1984, Neuroscience.

[52]  M Freedman,et al.  Amnesia after anterior communicating artery aneurysm rupture , 1984, Neurology.

[53]  D. Amaral,et al.  The distribution of acetylcholinesterase in the hippocampal formation of the monkey , 1984, The Journal of comparative neurology.

[54]  D. Benson,et al.  Amnesia with hippocampal lesions cardiopulmonary arrest , 1984, Neurology.

[55]  M. Mishkin,et al.  Visual recognition impairment following medial thalamic lesions in monkeys , 1983, Neuropsychologia.

[56]  C. Cavada,et al.  Allocortical afferent connections of the prefrontal cortex of the cat , 1983, Brain Research.

[57]  E. Irle,et al.  Widespread cortical projections of the hippocampal formation in the cat , 1982, Neuroscience.

[58]  P. Goldman-Rakic,et al.  Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response , 1982, Brain Research.

[59]  Hans J. Markowitsch,et al.  Thalamic mediodorsal nucleus and memory: A critical evaluation of studies in animals and man , 1982, Neuroscience & Biobehavioral Reviews.

[60]  S. Zola-Morgan,et al.  Hippocampal resections impair associative learning and recognition memory in the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  P. Goldman-Rakic,et al.  Spatial memory impairments following damage to the mediodorsal nucleus of the thalamus in rhesus monkeys , 1982, Brain Research.

[62]  M. Mesulam,et al.  Additional factors influencing sensitivity in the tetramethyl benzidine method for horseradish peroxidase neurohistochemistry. , 1980, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[63]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[64]  A. Mikami,et al.  Neuronal activity in the monkey dorsolateral prefrontal cortex during a discrimination task with delay , 1980, Brain Research.

[65]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[66]  W. Schwerdtfeger.  Direct efferent and afferent connections of the hippocampus with the neocortex in the marmoset monkey. , 1979, The American journal of anatomy.

[67]  M. Sugishita,et al.  Pure memory loss with hippocampal lesions: a pneumoencephalographic study. , 1979, Archives of neurology.

[68]  F. Gallyas.  Silver staining of myelin by means of physical development. , 1979, Neurological research.

[69]  G. V. Van Hoesen,et al.  Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. , 1977, Science.

[70]  R. Morawetz,et al.  The Anterior Communicating Artery Has Significant Branches , 1977, Stroke.

[71]  J. Fuster,et al.  Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. , 1976, Journal of comparative and physiological psychology.

[72]  H. D. Steklis,et al.  A neural substrate for affiliative behavior in nonhuman primates. , 1976, Brain, behavior and evolution.

[73]  J. Fuster.  Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[74]  H. Mahut,et al.  A selective spatial deficit in monkeys after transection of the fornix. , 1972, Neuropsychologia.

[75]  W. Nauta,et al.  Neural associations of the frontal cortex. , 1972, Acta neurobiologiae experimentalis.

[76]  H. Mahut.  Spatial and object reversal learning in monkeys with partial temporal lobe ablations. , 1971, Neuropsychologia.

[77]  W. Nauta.  The problem of the frontal lobe: a reinterpretation. , 1971, Journal of psychiatric research.

[78]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[79]  "Pure" memory loss with hippocampal lesions: a case report. , 1968, Transactions of the American Neurological Association.

[80]  Sweet Wh,et al.  Amnesic syndrome with anterior communicating artery aneurysm. , 1967 .

[81]  W. Sweet,et al.  AMNESIC SYNDROME WITH ANTERIOR COMMUNICATING ARTERY ANEURYSM , 1967, The Journal of nervous and mental disease.

[82]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[83]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[84]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[85]  C. Jacobsen,et al.  Studies of cerebral function in primates. I. The functions of the frontal association areas in monkeys. , 1936 .