Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation

Rats with dorsal hippocampus or associative parietal cortex (APC) lesions and sham-operated controls were trained on variants of the Morris water maze navigation task. In the 'proximal landmark condition', the rats had to localize the hidden platform solely on the basis of three salient object landmarks placed directly in the swimming pool. In the 'distal landmark condition', rats could rely only on distal landmarks (room cues) to locate the platform. In the 'beacon condition', the platform location was signaled by a salient cue directly attached to it. Rats with hippocampal lesions were impaired in the distal and to a less extent in the proximal landmark condition whereas rats with parietal lesions were impaired only in the proximal landmark condition. None of the lesioned groups was impaired in the beacon condition. These results suggest that the processing of information related to proximal, distal landmarks or associated beacon are mediated by different neural systems. The hippocampus would contribute to both proximal and distal landmark processing whereas the APC would be involved in the processing of proximal landmarks only. Navigation relying on a cued-platform would not require participation of the hippocampus nor the APC. Assuming that the processing of proximal landmarks heavily depends on the integration of visuospatial and idiothetic information, these results are consistent with the hypothesis that the APC plays a role in the combination of multiple sensory information and contributes to the formation of an allocentric spatial representation.

[1]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  C. Thinus-Blanc,et al.  A study of exploratory behavior as an index of spatial knowledge in hamsters , 1986 .

[3]  R. J. McDonald,et al.  Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. , 1994, Cerebral cortex.

[4]  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 .

[5]  R. Morris,et al.  Allocentric Spatial Learning by Hippocampectomised Rats: A Further Test of the “Spatial Mapping” and “Working Memory” Theories of Hippocampal Function , 1986, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[6]  E Save,et al.  Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. , 1992, Behavioral neuroscience.

[7]  E. J. Green,et al.  Cortical representation of motion during unrestrained spatial navigation in the rat. , 1994, Cerebral cortex.

[8]  I. Whishaw,et al.  Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  R. Muller,et al.  Failure of Centrally Placed Objects to Control the Firing Fields of Hippocampal Place Cells , 1997, The Journal of Neuroscience.

[10]  Nigel Foreman,et al.  Exploratory activity and response to a spatial change in rats with hippocampal or posterior parietal cortical lesions , 1992, Behavioural Brain Research.

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

[12]  Francis Boon,et al.  Navigation in the water maze: The role of proximal and distal visual cues, path integration, and magnetic field information , 1997, Psychobiology.

[13]  C. Thinus-Blanc,et al.  A Study of Spatial Parameters Encoded During Exploration in Hamsters , 1987 .

[14]  Etienne Save,et al.  The differences shown by C57BL/6 and DBA/2 inbred mice in detecting spatial novelty are subserved by a different hippocampal and parietal cortex interplay , 1996, Behavioural Brain Research.

[15]  I. Whishaw Hippocampal, granule cell and CA3–4 lesions impair formation of a place learning-set in the rat and induce reflex epilepsy , 1987, Behavioural Brain Research.

[16]  Simon Benhamou,et al.  LANDMARK USE BY NAVIGATING RATS (RATTUS NORVEGICUS) : CONTRASTING GEOMETRIC AND FEATURAL INFORMATION , 1998 .

[17]  L. Jarrard On the role of the hippocampus in learning and memory in the rat. , 1993, Behavioral and neural biology.

[18]  I. Whishaw,et al.  Recovery from early cortical lesions in rats: 6. Cortical noradrenaline, cortical thickness, and development of spatial learning after frontal lesions or hemidecortications , 1989, Psychobiology.

[19]  Animal spatial cognition and exploration. , 1998 .

[20]  R. Kesner,et al.  Spatial cognitive maps: differential role of parietal cortex and hippocampal formation. , 1988, Behavioral neuroscience.

[21]  B. Kolb,et al.  Behavioural and anatomical studies of the posterior parietal cortex in the rat , 1987, Behavioural Brain Research.

[22]  On the spatial information used by the neural substrates of navigation , 1998 .

[23]  E. Save,et al.  The contribution of the associative parietal cortex and hippocampus to spatial processing in rodents , 1998, Psychobiology.

[24]  R Biegler,et al.  Landmark stability: studies exploring whether the perceived stability of the environment influences spatial representation. , 1996, The Journal of experimental biology.

[25]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[26]  H. Rouanet,et al.  COMPARISON BETWEEN TREATMENTS IN A REPEATED‐MEASUREMENT DESIGN: ANOVA AND MULTIVARIATE METHODS , 1970 .

[27]  L. Jarrard,et al.  Selective hippocampal lesions and behavior: effects of kainic acid lesions on performance of place and cue tasks. , 1983, Behavioral neuroscience.

[28]  G. Handelmann,et al.  Hippocampal function: Working memory or cognitive mapping? , 1980 .

[29]  E. Save,et al.  Spatial Firing of Hippocampal Place Cells in Blind Rats , 1998, The Journal of Neuroscience.

[30]  R. Sutherland,et al.  A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. , 1983, Behavioral neuroscience.

[31]  R. Muller,et al.  Further study of the control of place cell firing by intra‐apparatus objects , 1999, Hippocampus.

[32]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[33]  R. Kesner,et al.  The effects of dorsal versus ventral hippocampal, total hippocampal, and parietal cortex lesions on memory for allocentric distance in rats. , 1996, Behavioral neuroscience.

[34]  I. Whishaw,et al.  Recovery from early cortical lesions in rats. III. Neonatal removal of posterior parietal cortex has greater behavioral and anatomical effects than similar removals in adulthood , 1987, Behavioural Brain Research.

[35]  B Poucet,et al.  The neuropsychology of spatial cognition in the rat. , 1997, Critical reviews in neurobiology.

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

[37]  E Save,et al.  Effects of lesions of the associative parietal cortex on the acquisition and use of spatial memory in egocentric and allocentric navigation tasks in the rat. , 1996, Behavioral neuroscience.

[38]  N. White,et al.  Parallel Information Processing in the Dorsal Striatum: Relation to Hippocampal Function , 1999, The Journal of Neuroscience.

[39]  T. Sakamoto,et al.  Effects of fimbria-fornix lesions on rats’ use of intramaze stimuli in the water maze , 1998, Psychobiology.