Anatomical Organization of the Parahippocampal‐Hippocampal Network

Abstract: The anatomical organization of the parahipppocampal‐hippocampal network indicates that it consists of different parallel circuits. Considering the topographical distribution of sensory cortical inputs, the hypothesis is that the major parallel circuits carry functionally different information. These functionally different parallel routes reach different portions of the hippocampal network along the longitudinal axis of all fields as well as along the perpendicularly oriented transverse axis of CA1 and the subiculum. In the remaining fields of the hippocampal formation, that is, the dentate gyrus and CA2/CA3, separation along the transverse axis is not present. By contrast, here the functionally different pathways converge onto the same neuronal population. The entorhinal cortex holds a pivotal position among the cortices that make up the parahippocampal region. By way of the networks of the superficial and deep layers, it mediates, respectively, the input and output streams of the hippocampal formation. Moreover, the intrinsic entorhinal network, particularly the interconnections between the deep and superficial layers, may mediate the comparison of hippocampal input and output signals. As such, the entorhinal cortex may form part of a novelty detection network. In addition, the organization of the entorhinal‐hippocampal network may facilitate the holding of information. Finally, the terminal organization of the presubicular input to the medial entorhinal cortex indicates that the interactions between the deep and superficial entorhinal layers may be influenced by this input.

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

[2]  D. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents , 1975, Brain Research.

[3]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections , 1975, Brain Research.

[4]  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.

[5]  O. Steward,et al.  Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat , 1976, The Journal of comparative neurology.

[6]  O. Steward,et al.  Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat , 1976, The Journal of comparative neurology.

[7]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[8]  B. McNaughton,et al.  Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat , 1977, The Journal of comparative neurology.

[9]  A. Routtenberg,et al.  Topography between the entorhinal cortex and the dentate septotemporal axis in rats: I. Medial and intermediate entorhinal projecting cells , 1982, The Journal of comparative neurology.

[10]  G. V. Hoesen,et al.  A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat , 1983, Brain Research.

[11]  M P Witter,et al.  Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat , 1984, The Journal of comparative neurology.

[12]  C. Köhler Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex , 1985, The Journal of comparative neurology.

[13]  M. Witter A survey of the anatomy of the hippocampal formation, with emphasis on the septotemporal organization of its intrinsic and extrinsic connections. , 1986, Advances in experimental medicine and biology.

[14]  M P Witter,et al.  The organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat: I. A neuroanatomical tracing study , 1986, The Journal of comparative neurology.

[15]  F. L. D. Silva,et al.  Organization of the reciprocal connections between the subiculum and the enthorhinal cortex in the cat: II. An electrophysiological study , 1986, The Journal of comparative neurology.

[16]  M. Witter,et al.  Connections of the parahippocampal cortex in the cat. V. Intrinsic connections; comments on input/output connections with the hippocampus , 1986, The Journal of comparative neurology.

[17]  H. Groenewegen,et al.  Connections of the parahippocampal cortex. I. Cortical afferents , 1986, The Journal of comparative neurology.

[18]  M. Witter,et al.  Connections of the parahippocampal cortex in the cat. III. Cortical and thalamic efferents , 1986, The Journal of comparative neurology.

[19]  D. Amaral,et al.  The entorhinal cortex of the monkey: III. Subcortical afferents , 1987, The Journal of comparative neurology.

[20]  Nobuaki Tamamaki,et al.  Columnar organization in the subiculum formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus , 1987, Brain Research.

[21]  D. Amaral,et al.  The entorhinal cortex of the monkey: I. Cytoarchitectonic organization , 1987, The Journal of comparative neurology.

[22]  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.

[23]  Menno P. Witter,et al.  Entorhinal projections to the hippocampal CA1 region in the rat: An underestimated pathway , 1988, Neuroscience Letters.

[24]  A. Routtenberg,et al.  Topographical relationship between the entorhinal cortex and the septotemporal axis of the dentate gyrus in rats: II. Cells projecting from lateral entorhinal subdivision , 1988, The Journal of comparative neurology.

[25]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[26]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[27]  D. Amaral,et al.  Topographical organization of the entorhinal projection to the dentate gyrus of the monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. P. Witter,et al.  Connectivity of the rat hippocampus , 1989 .

[29]  Nobuaki Tamamaki,et al.  Disposition of the slab‐like modules formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus , 1990, The Journal of comparative neurology.

[30]  T. van Groen,et al.  Extrinsic projections from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections , 1990, The Journal of comparative neurology.

[31]  D. Amaral,et al.  Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE , 1990, Neuroscience Letters.

[32]  D. Amaral,et al.  Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex , 1991, The Journal of comparative neurology.

[33]  D. Amaral,et al.  Organization of CA1 projections to the subiculum: A PHA‐L analysis in the rat , 1991, Hippocampus.

[34]  I. Ferrer,et al.  Parvalbumin and calbindin D-28K in the human entorhinal cortex. An immunohistochemical study , 1992, Brain Research.

[35]  J. Michael Wyass,et al.  Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review , 1992, Hippocampus.

[36]  N. Tamamaki,et al.  Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure‐injection of neurobiotin , 1993, Hippocampus.

[37]  H. Braak,et al.  Parvalbumin‐immunoreactive structures of the adult human entorhinal and transentorhinal region , 1993, Hippocampus.

[38]  M. Witter Organization of the entorhinal—hippocampal system: A review of current anatomical data , 1993, Hippocampus.

[39]  W. Levy,et al.  Ultrastructural identification of entorhinal cortical synapses in CA1 stratum lacunosum‐moleculare of the rat , 1994, Hippocampus.

[40]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[41]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  M. Witter,et al.  Quantitative morphological analysis of subicular terminals in the rat entorhinal cortex , 1995, Hippocampus.

[43]  R. Llinás,et al.  Intracellular study of direct entorhinal inputs to field CA1 in the isolated guinea pig brain in vitro , 1995, Hippocampus.

[44]  M. Witter,et al.  Parvalbumin-immunoreactive neurons in the entorhinal cortex of the rat: localization, morphology, connectivity and ultrastructure , 1995, Journal of neurocytology.

[45]  N. Tamamaki,et al.  Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats , 1995, The Journal of comparative neurology.

[46]  R. Insausti,et al.  The human entorhinal cortex: A cytoarchitectonic analysis , 1995, The Journal of comparative neurology.

[47]  L. Leung Simulation of perforant path evoked field and intracellular potentials in hippocampal CA1 area , 1995, Hippocampus.

[48]  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.

[49]  M. Yeckel,et al.  Monosynaptic excitation of hippocampal CA1 pyramidal cells by afferents from the entorhinal cortex , 1995, Hippocampus.

[50]  M. Witter,et al.  Entorhinal-Hippocampal Interactions Revealed by Real-Time Imaging , 1996, Science.

[51]  D. Bilkey,et al.  Direct connection between perirhinal cortex and hippocampus is a major constituent of the lateral perforant path , 1998, Hippocampus.

[52]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[53]  W. Staines,et al.  Efferent projections of the anterior perirhinal cortex in the rat , 1996, The Journal of comparative neurology.

[54]  D. Bilkey,et al.  Current source density analysis of the potential evoked in hippocampus by perirhinal cortex stimulation , 1997, Hippocampus.

[55]  K. J. Canning,et al.  Lateral entorhinal, perirhinal, and amygdala‐entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: A current source density study , 1998, Hippocampus.

[56]  M. Witter,et al.  Parallel input to the hippocampal memory system through peri‐ and postrhinal cortices , 1997, Neuroreport.

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

[58]  A. Alonso,et al.  Muscarinic Induction of Synchronous Population Activity in the Entorhinal Cortex , 1997, The Journal of Neuroscience.

[59]  A. Alonso,et al.  Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex , 1997, Hippocampus.

[60]  D. Amaral,et al.  Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 1998 .

[61]  D. Amaral,et al.  Entorhinal cortex of the rat: Topographic organization of the cells of origin of the perforant path projection to the dentate gyrus , 1998, The Journal of comparative neurology.

[62]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .

[63]  Comparison of the electrophysiology and morphology of layers III and II neurons of the rat medial entorhinal cortex in vitro , 1998, The European journal of neuroscience.

[64]  D. Amaral,et al.  Entorhinal cortex of the rat: Organization of intrinsic connections , 1998, The Journal of comparative neurology.

[65]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex , 1998, The Journal of comparative neurology.

[66]  M. Witter,et al.  Perirhinal cortex input to the hippocampus in the rat: evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study , 1999, The European journal of neuroscience.

[67]  Perirhinal cortex does not project to the dentate gyrus , 1999, Hippocampus.

[68]  M. Stewart Columnar activity supports propagation of population bursts in slices of rat entorhinal cortex , 1999, Brain Research.

[69]  M. Witter,et al.  Presubicular Input to the Dendrites of Layer‐V Entorhinal Neurons in the Rat , 2000, Annals of the New York Academy of Sciences.

[70]  F. H. Lopes da Silva,et al.  Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat , 2001, Hippocampus.

[71]  F. H. Lopes da Silva,et al.  Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum , 2001, Hippocampus.