Active Spatial Information Processing in the Septo‐Hippocampal System

The hippocampal formation (HF) receives the final outputs from all association cortices, and processes and integrates this diverse information. Our neurophysiological data in rats and monkeys suggest active selection of relevant sensory information in the HF. In an open field, rat HF neurons strengthened their sensitivity to more relevant variables among various movement variables such as movement speed, direction, and turning angle based on navigation contexts. The HF place‐related activity in the monkey, which rode on a movable cab, became obscure in passive translocation of a monkey by an experimenter. This suggests that the animal actively senses the environment surrounding it during spatial navigation, and that spatial correlates of HF neurons depend on this active sensing. In the monkey septal nuclei that receive hippocampal outputs, some neurons were differential to specific views from 4 specific locations in an experimental room (place‐differential responses). Multidimensional scaling (MDS) analysis of place‐differential responses indicated that the 4 locations represented in a 2‐dimensional virtual space at relative positions were similar to those in the real experimental room. This might be a neurophysiological basis of a cognitive map and path finding. These results are consistent with recent human PET studies that indicated HF involvement in recalling routes and landmarks. Thus, a cognitive mapping system represented in the HF plays a pivotal role in active computation for path finding. Hippocampus 1999;9:458–466. © 1999 Wiley‐Liss, Inc.

[1]  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.

[2]  C. A. Castro,et al.  Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. , 1989, Science.

[3]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  C. Gallistel,et al.  Heading in the rat: Determination by environmental shape , 1988 .

[6]  Rosaleen A. McCarthy,et al.  Topographic amnesia: spatial memory disorder, perceptual dysfunction, or category specific semantic memory impairment? , 1996 .

[7]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[8]  T. Ono,et al.  Task-dependent representations in rat hippocampal place neurons. , 1997, Journal of neurophysiology.

[9]  R. Hampson,et al.  Hippocampal place cells: stereotypy and plasticity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  J. O’Keefe,et al.  Hippocampal place units in the freely moving rat: Why they fire where they fire , 1978, Experimental Brain Research.

[11]  Joseph B. Travers,et al.  A metric for the breadth of tuning of gustatory neurons , 1979 .

[12]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[13]  T. Ono,et al.  Septal neuronal responses related to spatial representation in monkeys , 1997, Hippocampus.

[14]  Richard S. J. Frackowiak,et al.  Learning to find your way: a role for the human hippocampal formation , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[16]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  Hisao Nishijo,et al.  The relationship between monkey hippocampus place-related neural activity and action in space , 1997, Neuroscience Letters.

[18]  B. Poucet Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. , 1993, Psychological review.

[19]  A. Berthoz,et al.  Mental navigation along memorized routes activates the hippocampus, precuneus, and insula , 1997, Neuroreport.

[20]  Hisao Nishijo,et al.  Monkey hippocampal neuron responses related to spatial and non-spatial influence , 1993, Neuroscience Letters.

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

[22]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  H. Eichenbaum,et al.  Brain Aging: Changes in the Nature of Information Coding by the Hippocampus , 1997, The Journal of Neuroscience.

[24]  C. Thinus-Blanc,et al.  Route planning in cats, in relation to the visibility of the goal , 1983, Animal Behaviour.

[25]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 2004, Experimental Brain Research.

[26]  B. McNaughton,et al.  Cortical-hippocampal interactions and cognitive mapping: A hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing , 1989 .

[27]  L. Squire Memory and Brain , 1987 .

[28]  R. Hampson,et al.  Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. , 1993, Behavioral neuroscience.

[29]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  T. Ono,et al.  Place and contingency differential responses of monkey septal neurons during conditional place-object discrimination , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  B. McNaughton,et al.  Place cells, head direction cells, and the learning of landmark stability , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  T. Ono,et al.  Amygdalar and hippocampal neuron responses related to recognition and memory in monkey. , 1993, Progress in brain research.

[34]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[35]  M. D’Esposito,et al.  The Parahippocampus Subserves Topographical Learning in Man , 1996 .

[36]  K. Nakamura,et al.  Monkey hippocampal neurons related to spatial and nonspatial functions. , 1993, Journal of neurophysiology.

[37]  R. Biegler,et al.  Landmark stability is a prerequisite for spatial but not discrimination learning , 1993, Nature.

[38]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[39]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

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

[41]  A. Pickering,et al.  Spatial memory deficits in patients with unilateral damage to the right hippocampal formation , 1997, Neuropsychologia.

[42]  H. Eichenbaum,et al.  The hippocampus--what does it do? , 1992, Behavioral and neural biology.

[43]  L. Swanson,et al.  Structural Evidence for Functional Domains in the Rat Hippocampus , 1996, Science.

[44]  A. Sirigu,et al.  Pure Topographical Disorientation: A Definition and Anatomical Basis , 1987, Cortex.

[45]  E. Maguire,et al.  Topographical disorientation following unilateral temporal lobe lesions in humans , 1996, Neuropsychologia.

[46]  H Eichenbaum,et al.  Thinking about brain cell assemblies. , 1993, Science.

[47]  D. Benson,et al.  Loss of topographic familiarity. An environmental agnosia. , 1986, Archives of neurology.

[48]  R E Hampson,et al.  Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[50]  B. McNaughton,et al.  Dead Reckoning, Landmark Learning, and the Sense of Direction: A Neurophysiological and Computational Hypothesis , 1991, Journal of Cognitive Neuroscience.

[51]  H. Eichenbaum,et al.  Spatial and behavioral correlates of hippocampal neuronal activity , 1989 .

[52]  M. D’Esposito,et al.  Environmental Knowledge Is Subserved by Separable Dorsal/Ventral Neural Areas , 1997, The Journal of Neuroscience.

[53]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[54]  Taketoshi Ono,et al.  Place recognition responses of neurons in monkey hippocampus , 1991, Neuroscience Letters.

[55]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[56]  E Save,et al.  The effects of reversible inactivations of the hippocampus on exploratory activity and spatial memory , 1991, Hippocampus.

[57]  A. Etienne,et al.  The effect of a single light cue on homing behaviour of the golden hamster , 1990, Animal Behaviour.

[58]  H. Eichenbaum,et al.  Brain Aging: Impaired Coding of Novel Environmental Cues , 1997, The Journal of Neuroscience.

[59]  C. C. Wood,et al.  Task-dependent field potentials in human hippocampal formation , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  S Eifuku,et al.  Neuronal activity in the primate hippocampal formation during a conditional association task based on the subject's location , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .