Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T02:11:35.191Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatial Navigation in Rats and Humans: A Neuropsychological Perspective

Published online by Cambridge University Press:  17 May 2019

Ian Stuart Open the ORCID record for Ian Stuart [Opens in a new window]
Ian Stuart*
Affiliation:
Private Practice, Eastbourne House, East Melbourne, Victoria, Australia
*
*Corresponding author. Email: [email protected]
Get access

Abstract

Background and objective:

In a landmark publication, O’Keefe & Dostrovsky (1971) presented a model for spatial navigation in the rat, the cognitive map theory. In this theory they proposed that the processing and storage of spatial information for spatial navigation takes place in the hippocampus. The theory was extended to include the contribution of the grid cells in the medial entorhinal cortex (Hafting et al. 2005). The cognitive map theory has been widely applied to spatial navigation in humans as well as rats. In this paper, an alternative theory is proposed in which spatial processing takes place in the right parieto-temporo-occipital area in humans, and that damage to this area causes a fragmentation in the sense of space, affecting the recall of both visual and tactile spatial information.

Method:

A group of eight subjects with damage to the right parieto-temporo-occipital area and a fragmented sense of space was assessed on tests of spatial navigation and memory and the results were compared with a group of patients with damage to the right hippocampus. Other comparison groups included left and right hemisphere subjects with normal spatial functioning.

Results:

The results suggest that, in the human, damage to the right parieto-temporo-occipital area causes a fragmentation in the sense of space, as well as an impaired memory for spatial material in both the visual and tactile modalities. These results support a model of spatial navigation in which the integrity of the right parieto-temporo-occipital area, and not the right hippocampus, is a necessary condition for the processing of spatial information in humans. An alternative explanation for the functioning of the right hippocampus is also presented.

Keywords

Cognitive map theoryparietal lobehippocampusmotor learningspatial coordinate systemtopographical disorientation
Type
Articles
Information
Brain Impairment , Volume 20 , Issue 3 , December 2019 , pp. 251 - 267
Copyright
© Australasian Society for the Study of Brain Impairment 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersen, R. (1997). Multimodal integration for the representation of space in the posterior parietal cortex. Philosophical Transactions of the Royal Society B, 352, 1421–1428.CrossRefGoogle ScholarPubMed
Banta Lavenex, P. A., Colombo, F., Ribordy Lambert, F., & Lavenex, P. (2014). The human hippocampus beyond the cognitive map: Evidence from a densely amnesic patient. Frontiers in Human Neuroscience, 8, 711. doi: 10.3389/fnhum.2014.00711 CrossRefGoogle ScholarPubMed
Benton, A. L., & Fogel, M. L. (1962). Three-dimensional constructional praxis. A clinical test. Archives of Neurology, 7, 347–354.CrossRefGoogle ScholarPubMed
Bohbot, V. D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., & Nadel, L. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia, 36(11), 1217–1238.CrossRefGoogle ScholarPubMed
Buneo, C. A., & Andersen, R. A. (2006). The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia, 44(13), 2594–2606. doi: 10.1016/j.neuropsychologia.2005.10.011 CrossRefGoogle ScholarPubMed
Burgess, N., Maguire, E. A., & O’Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35(4), 625–641.CrossRefGoogle ScholarPubMed
Burgess, N., & O’Keefe, J. (2003). Neural representations in human spatial memory. Trends in Cognitive Sciences, 7(12), 517–519.CrossRefGoogle ScholarPubMed
Corkin, S. (1965). Tactually guided maze learning in man: Effects of unilateral cortical excisions and bilateral hippocampal lesions. Neuropsychologia, 3, 339–351.CrossRefGoogle Scholar
Cui, H. (2014). From intention to action: Hierarchical sensorimotor transformation in the posterior parietal Cortex. eNeuro, 1(1). doi: 10.1523/ENEURO.0017-14.2014 CrossRefGoogle ScholarPubMed
Dupret, D., O’Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010). The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nature Neuroscience, 13(8), 995–1002. doi: 10.1038/nn.2599 CrossRefGoogle ScholarPubMed
Ego-Stengel, V., & Wilson, M. A. (2010). Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus, 20(1), 1–10. doi: 10.1002/hipo.20707 Google ScholarPubMed
Ekstrom, A. D., Kahana, M. J., Caplan, J. B., Fields, T. A., Isham, E. A., Newman, E. L., & Fried, I. (2003). Cellular networks underlying human spatial navigation. Nature, 425(6954), 184–188. doi: 10.1038/nature01964 CrossRefGoogle ScholarPubMed
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsaki, G., & Zugaro, M. B. (2009). Selective suppression of hippocampal ripples impairs spatial memory. Nature Neuroscience, 12(10), 1222–1223. doi: 10.1038/nn.2384 CrossRefGoogle ScholarPubMed
Haaland, K., Harrington, D., & Knight, R. (2000). Neural representations of skilled movement. Brain, 123, 2306–2313.CrossRefGoogle ScholarPubMed
Hafting, T., Fyhn, M., Molden, S., Moser, M. B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052), 801–806. doi: 10.1038/nature03721 CrossRefGoogle ScholarPubMed
Hales, J. B., Schlesiger, M. I., Leutgeb, J. K., Squire, L. R., Leutgeb, S., & Clark, R. E. (2014). Medial entorhinal cortex lesions only partially disrupt hippocampal place cells and hippocampus-dependent place memory. Cell Reports, 9(3), 893–901. doi: 10.1016/j.celrep.2014.10.009 CrossRefGoogle ScholarPubMed
Hartley, T., Lever, C., Burgess, N., & O’Keefe, J. (2014). Space in the brain: How the hippocampal formation supports spatial cognition. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 369(1635), 20120510. doi: 10.1098/rstb.2012.0510 CrossRefGoogle ScholarPubMed
Hassabis, D., Chu, C., Rees, G., Weiskopf, N., Molyneux, P. D., & Maguire, E. A. (2009). Decoding neuronal ensembles in the human hippocampus. Current Biology, 19(7), 546–554. doi: 10.1016/j.cub.2009.02.033 CrossRefGoogle ScholarPubMed
Hécaen, H., Penfield, W., Bertrand, C., & Malmo, R. (1956). The syndrome of apractognosia due to lesions of the minor cerebral hemisphere. Archives of Neurology and Psychiatry, 75, 400–434.CrossRefGoogle ScholarPubMed
Howard, L. R., Javadi, A. H., Yu, Y., Mill, R. D., Morrison, L. C., Knight, R., … Spiers, H. J. (2014). The hippocampus and entorhinal cortex encode the path and Euclidean distances to goals during navigation. Current Biology, 24(12), 1331–1340. doi: 10.1016/j.cub.2014.05.001 CrossRefGoogle ScholarPubMed
Jancke, L., Kleinschmidt, A.,Mirzazade, S., Shah, N., & Freund, H.-J. (2001). The role of the inferior parietal corex in linking the tactile perception and manual construction of object shapes. Cerebral Cortex, 11, 114–121.CrossRefGoogle Scholar
Lee, A. K., & Wilson, M. A. (2002). Memory of sequential experience in the hippocampus during slow wave sleep. Neuron, 36(6), 1183–1194.CrossRefGoogle ScholarPubMed
Lewis, D. (1972). We, the navigators. South Australia: Griffin Press.Google Scholar
Maguire, E. A., Burgess, N., Donnett, J. G., Frackowiak, R. S., Frith, C. D., & O’Keefe, J. (1998). Knowing where and getting there: a human navigation network. Science, 280(5365), 921–924.CrossRefGoogle ScholarPubMed
Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016). Hippocampo-cortical coupling mediates memory consolidation during sleep. Nature Neuroscience, 19(7), 959–964. doi: 10.1038/nn.4304 CrossRefGoogle ScholarPubMed
Matsui, T., & Hirano, A. (1978). An atlas of the human brain for computerized tomography. Tokyo: Igaku-Shoin Ltd.Google Scholar
McFie, J., Piercy, M., & Zangwill, O. (1950). Visuo-spatial agnosia associated with lesion of the right cerebral hemisphere. Brain, 733, 167–190.CrossRefGoogle Scholar
Milner, B. (1965). Visually guided maze learning in man: effects of hippocampal, bilateral frontal and unilateral cerebral lesions. Neuropsychologia, 3, 317–338.CrossRefGoogle Scholar
Milner, B. (1966). Amnesia following operation on the temporal lobes. In Whitty, C. & Zangwill, O. (Eds.), Amnesia (pp. 109–132), London: Butterworths.Google Scholar
Morris, R. G., Garrud, P., Rawlins, J. N., & O’Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681–683.CrossRefGoogle ScholarPubMed
Moser, E. I., Kropff, E., & Moser, M. B. (2008). Place cells, grid cells, and the brain’s spatial representation system. Annual Review of Neuroscience, 31, 69–89. doi: 10.1146/annurev.neuro.31.061307.090723 CrossRefGoogle ScholarPubMed
O’Keefe, J. (1991). An allocentric spatial model for the hippocampal cognitive map. Hippocampus, 1(3), 230–235. doi: 10.1002/hipo.450010303 CrossRefGoogle ScholarPubMed
O’Keefe, J. (2014). Nobel lecture: spatial cells in the hippocampal formation. Retrieved from http://www.nobelprize.org/nobel_prizes/medicine/laureates/2014/okeefe-lecture.html Google Scholar
O’Keefe, J., & Burgess, N. (1999). Theta activity, virtual navigation and the human hippocampus. Trends in Cognitive Sciences, 3(11), 403–406.CrossRefGoogle ScholarPubMed
O’Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34(1), 171–175.CrossRefGoogle ScholarPubMed
O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon Press.Google Scholar
Paillard, J. (1971). Les determinants moteur de l’organisation de l’espace. Cahiers de Psychologie, 14(4), 261–316.Google Scholar
Paterson, A., & Zangwill, O. (1944). Disorders of visual space perception associated with lesions of the right cerebral hemisphere. Brain, 67, 331–358.CrossRefGoogle Scholar
Paterson, A., & Zangwill, O. (1945). A case of topographical disorientation associated with a unilateral cerebral lesion. Brain, 68, 188–211.CrossRefGoogle ScholarPubMed
Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., & Battaglia, F. P. (2009). Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nature Neuroscience, 12(7), 919–926. doi: 10.1038/nn.2337 CrossRefGoogle ScholarPubMed
Piaget, J., & Inhelder, B. (1956). The child’s conception of space. London: Routledge and Kegan Paul.Google Scholar
Piaget, J., & Inhelder, B. (1971). Mental imagery in the child. London: Routledge and Kegan Paul.Google Scholar
Potgieser, A., van der Hoorn, A., & de Jong, B. (2015). Cerebral activations related to writing and drawing with each hand. PLoS ONE, 10(5). doi: 10.1371/journal.pone.0126723 CrossRefGoogle ScholarPubMed
Qin, Y. L., McNaughton, B. L., Skaggs, W. E., & Barnes, C. A. (1997). Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philosophical Transactions of the Royal Society of London B, Biological Sciences, 352(1360), 1525–1533. doi: 10.1098/rstb.1997.0139 CrossRefGoogle ScholarPubMed
Ranck, J. B. Jr. (1984). Head direction cells in the deep cell layers of dorsal presubiculum in freely-moving rats. Society for Neuroscience Abstracts, 10, 599.Google Scholar
Rey, A. (1959). Manuel: Test de copie d’une figure complexe de A Rey. Paris: Les editions du centre de psychologie appliquee.Google Scholar
Rothschild, G., Eban, E., & Frank, L. M. (2017). A cortical-hippocampal-cortical loop of information processing during memory consolidation. Nature Neuroscience, 20(2), 251–259. doi: 10.1038/nn.4457 CrossRefGoogle ScholarPubMed
Seitz, R. J., Canavan, A. G., Yaguez, L., Herzog, H., Tellmann, L., Knorr, U., … Homberg, V. (1997). Representations of graphomotor trajectories in the human parietal cortex: Evidence for controlled processing and automatic performance. European Journal of Neuroscience, 9(2), 378–389.CrossRefGoogle ScholarPubMed
Semmes, J. (1965). A non-tactual factor in astereognosis. Neuropsychologia, 3, 295–315.CrossRefGoogle Scholar
Semmes, J., Weinstein, S., Ghent, L., & Teuber, H.-L. (1955). Spatial orientation in man after cerebral injury: Part 1. Analysis by locus of lesion. Journal of Psychology, 39, 295–315.Google Scholar
Skaggs, W. E., & McNaughton, B. L. (1996). Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science, 271(5257), 1870–1873.CrossRefGoogle ScholarPubMed
Spiers, H. J., & Maguire, E. A. (2006). Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage, 31(4), 1826–1840. doi: 10.1016/j.neuroimage.2006.01.037 CrossRefGoogle ScholarPubMed
Stark, C. (2007). Functional role of the human hippocampus. In Andersen, P., Morris, R., Amaral, D. G., Bliss, T. V., & O“Keefe, J. (Eds.), The hippocampus book (pp. 549–579), Oxford; New York: Oxford University Press.Google Scholar
Steffenach, H. A., Witter, M., Moser, M. B., & Moser, E. I. (2005). Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron, 45(2), 301–313. doi: 10.1016/j.neuron.2004.12.044 CrossRefGoogle ScholarPubMed
Stuart, I. (1989). Spatial orientation in the congenitally blind (Unpublished doctoral thesis PhD), University of Melbourne.Google Scholar
Stuart, I. (1995). Spatial orientation and congenital blindness: A neuropsychological approach. Journal of Visual Impairment and Blindness, 89, 129–141.Google Scholar
Taube, J. S. (2007). The head direction signal: origins and sensory-motor integration. Annual Review of Neuroscience, 30, 181–207. doi: 10.1146/annurev.neuro.29.051605.112854 CrossRefGoogle ScholarPubMed
Taube, J. S., Muller, R. U., & Ranck, J. B. Jr. (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. The Journal of Neuroscience, 10(2), 420–435.CrossRefGoogle Scholar
Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 40, 60–70.CrossRefGoogle Scholar
Wechsler, D. (1987). Wechsler Memory Scale-Revised. San Antonio: The Psychological Corporation. Harcourt Brace Jovanovich.Google Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale-Third Edition. New York: Psychological Corporation.Google Scholar
Wilber, A. A., Skelin, I., Wu, W., & McNaughton, B. L. (2017). Laminar organization of encoding and memory reactivation in the parietal cortex. Neuron, 95(6), 1406-1419.e1405. doi: 10.1016/j.neuron.2017.08.033 CrossRefGoogle ScholarPubMed
Wilson, M. A., & McNaughton, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science, 265(5172), 676–679.CrossRefGoogle ScholarPubMed