Hippocampus, space, and memory
Abstract
We examine two different descriptions of the behavioral functions of the hippocampal system. One emphasizes spatially organized behaviors, especially those using cognitive maps. The other emphasizes memory, particularly working memory, a short-term memory that requires iexible stimulus-response associations and is highly susceptible to interference. The predictive value of the spatial and memory descriptions were evaluated by testing rats with damage to the hippocampal system in a series of experiments, independently manipulating the spatial and memory characteristics of a behavioral task. No dissociations were found when the spatial characteristics of the stimuli to be remembered were changed; lesions produced a similar deficit in both spatial and nonspatial test procedures, indicating that the hippocampus was similarly involved regardless of the spatial nature of the task. In contrast, a marked dissociation was found when the memory requirements were altered. Rats with lesions were able to perform accurately in tasks that could be solved exclusively on the basis of reference memory. They performed at chance levels and showed no signs of recovery even with extensive postoperative training in tasks that required working memory. In one experiment all the characteristics of the reference memory and working memory procedures were identical except the type of memory required. Consequently, the behavioral dissociation cannot be explained by differences in attention, motivation, response inhibition, or the type of stimuli to be remembered. As a result of these experiments we propose that the hippocampus is selectively involved in behaviors that require working memory, irrespective of the type of material (spatial or nonspatial) that is to be processed by that memory.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Unlike stress, hippocampal lesion or inactivation produces a general impairment of spatial learning and memory in rats.
“Empirical support for this idea is the finding that, unlike stress, hippocampal lesion or inactivation produces a general impairment of spatial learning and memory in rats (O'Keefe and Nadel [278]; Olton et al. [279]; Steele and Morris [280]; Diamond et al. [52]; Morris et al. [281]; Nakazawa et al. [282]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Olton et al. [279]
Cites
REMEMBERING: A STUDY IN EXPERIMENTAL AND SOCIAL PSYCHOLOGY
Bartlett, F. C., & Burt, C. (1933) · British Journal of Educational Psychology · doi:10.1111/j.2044-8279.1933.tb02913.x · Cited by 7,475 · see citing works
Optimal foraging, the marginal value theorem
Charnov, E. L. (1976) · Theoretical Population Biology · doi:10.1016/0040-5809(76)90040-x · Cited by 5,374 · see citing works
Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.
Milner, B., Corkin, S., & Teuber, H.-L. (1968) · Neuropsychologia · doi:10.1016/0028-3932(68)90021-3 · Cited by 1,229 · see citing works
THE NEUROANATOMY OF AMNESIA: A CRITIQUE OF THE HIPPOCAMPAL MEMORY HYPOTHESIS
HOREL, J. A. (1978) · Brain · doi:10.1093/brain/101.3.403 · Cited by 493 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · see citing works
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
Gray, J. A. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00013066 · Cited by 4,477 · see citing works
The Medial Temporal Lobe Memory System
Squire, L. R., & Zola-Morgan, S. (1991) · Science · doi:10.1126/science.1896849 · Cited by 3,282 · see citing works
A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data
Ennaceur, A., & Delacour, J. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90157-x · Cited by 3,223 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Spatial localization does not require the presence of local cues
Morris, R. G. M. (1981) · Learning and Motivation · doi:10.1016/0023-9690(81)90020-5 · Cited by 2,699 · see citing works
The Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Zola-Morgan, S., Squire, L., & Amaral, D. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02950.1986 · Cited by 1,997 · see citing works
Episodic memory, amnesia, and the hippocampal–anterior thalamic axis
Aggleton, J. P., & Brown, M. W. (1999) · Behavioral and Brain Sciences · doi:10.1017/s0140525x99002034 · Cited by 1,879 · see citing works
How many memory systems are there?
Tulving, E. (1985) · American Psychologist · doi:10.1037/0003-066x.40.4.385 · Cited by 1,909 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
The principal features and mechanisms of dopamine modulation in the prefrontal cortex
Seamans, J. K., & Yang, C. R. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.05.006 · Cited by 1,592 · see citing works
Regional dissociations within the hippocampus-memory and anxiety
Bannerman, D. M., Rawlins, J. N. P., McHugh, S. B., Deacon, R. M. J., Yee, B. K., Bast, T., Zhang, W.-N., Pothuizen, H. H. J., & Feldon, J. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.03.004 · Cited by 1,462 · see citing works
Brain Systems that Mediate both Emotion and Cognition
Gray, J. A. (1990) · Cognition & Emotion · doi:10.1080/02699939008410799 · Cited by 1,400 · see citing works
CENTRAL CHOLINERGIC SYSTEMS AND COGNITION
Everitt, B. J., & Robbins, T. W. (1997) · Annual Review of Psychology · doi:10.1146/annurev.psych.48.1.649 · Cited by 1,348 · see citing works
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134 · see citing works
On the role of the hippocampus in learning and memory in the rat.
Jarrard, L. E. (1993) · Behavioral and Neural Biology · doi:10.1016/0163-1047(93)90664-4 · Cited by 1,125 · see citing works
The Hippocampus, Memory, and Place Cells
Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M., & Tanila, H. (1999) · Neuron · doi:10.1016/s0896-6273(00)80773-4 · Cited by 1,064 · see citing works
Effect of Neonatal Handling on Age-Related Impairments Associated with the Hippocampus
Meaney, M. J., Aitken, D. H., van Berkel, C., Bhatnagar, S., & Sapolsky, R. M. (1988) · Science · doi:10.1126/science.3340858 · Cited by 1,074 · see citing works
The acute effects of corticosteroids on cognition: integration of animal and human model studies
LUPIEN, S., & MCEWEN, B. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00004-0 · Cited by 1,024 · see citing works
The default mode network in cognition: a topographical perspective
Smallwood, J., Bernhardt, B. C., Leech, R., Bzdok, D., Jefferies, E., & Margulies, D. S. (2021) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00474-4 · Cited by 935 · see citing works
Awake hippocampal sharp-wave ripples support spatial memory
Jadhav, S. P., Kemere, C., German, P. W., & Frank, L. M. (2012) · Science · doi:10.1126/science.1217230 · Cited by 924 · see citing works
Richardson-Klavehn, A., & Bjork, R. A. (1988) · Annual Review of Psychology · doi:10.1146/annurev.ps.39.020188.002355 · Cited by 983 · see citing works
Brain connectivity related to working memory performance
Hampson, M., Driesen, N. R., Skudlarski, P., Gore, J. C., & Constable, R. T. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3408-06.2006 · Cited by 853 · see citing works
Reversal of learning deficits in a Tsc2+/− mouse model of tuberous sclerosis
Ehninger, D., Han, S., Shilyansky, C., Zhou, Y., Li, W., Kwiatkowski, D. J., Ramesh, V., & Silva, A. J. (2008) · Nature Medicine · doi:10.1038/nm1788 · Cited by 879 · see citing works
The hippocampus—what does it do?
Eichenbaum, H., Otto, T., & Cohen, N. J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90724-i · Cited by 867 · see citing works
Précis of Elements of episodic memory
Tulving, E. (1984) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0004440x · Cited by 809 · see citing works
Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition
Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., & Buzsáki, G. (2012) · Nature Neuroscience · doi:10.1038/nn.3077 · Cited by 728 · see citing works
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“[279]; Steele and Morris [280]; Diamond et al.”
BackgroundWebster, S. J., Bachstetter, A. D., Nelson, P. T., Schmitt, F. A., & Van Eldik, L. J. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00088 · Cited by 755 · see citing works
“A more complex maze type task used to test murine spatial working memory is that of the Radial Arm Maze (RAM), consisting of several arms (usually 6–8) radiating outwards from a central platform (Olton and Samuelson, 1976; Olton et al., 1979).”
MethodSolomon, P. R., Vander Schaaf, E. R., Thompson, R. F., & Weisz, D. J. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.5.729 · Cited by 724 · see citing works
Squire, L. R., Genzel, L., Wixted, J. T., & Morris, R. G. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021766 · Cited by 700 · see citing works
One-trial object recognition in rats and mice: Methodological and theoretical issues
Ennaceur, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.036 · Cited by 676 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Ennaceur, A., Neave, N., & Aggleton, J. P. (1997) · Experimental Brain Research · doi:10.1007/pl00005603 · Cited by 670 · see citing works
Glucocorticoids and the regulation of memory consolidation
Roozendaal, B. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00058-x · Cited by 665 · see citing works
The neuropsychology of 3-D space.
Previc, F. H. (1998) · Psychological Bulletin · doi:10.1037/0033-2909.124.2.123 · Cited by 604 · see citing works
Associations across time: The hippocampus as a temporary memory store
Rawlins, J. N. P. (1985) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00001291 · Cited by 561 · see citing works
Fuchs, E. C., Zivkovic, A. R., Cunningham, M. O., Middleton, S., LeBeau, F. E. N., Bannerman, D. M., Rozov, A., Whittington, M. A., Traub, R. D., Rawlins, J. N. P., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.031 · Cited by 532 · see citing works
Bohbot, V. D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., & Nadel, L. (1998) · Neuropsychologia · doi:10.1016/s0028-3932(97)00161-9 · Cited by 516 · see citing works
Sleep states and memory processes
Smith, C. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00024-n · Cited by 473 · see citing works
The case of K.C.: contributions of a memory-impaired person to memory theory
Rosenbaum, R. S., Köhler, S., Schacter, D. L., Moscovitch, M., Westmacott, R., Black, S. E., Gao, F., & Tulving, E. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.10.007 · Cited by 433 · see citing works
The cognitive atlas: toward a knowledge foundation for cognitive neuroscience
Poldrack, R. A., Kittur, A., Kalar, D., Miller, E., Seppa, C., Gil, Y., Parker, D. S., Sabb, F. W., & Bilder, R. M. (2011) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2011.00017 · Cited by 385 · see citing works
The Role of Hippocampal Replay in Memory and Planning
Ólafsdóttir, H. F., Bush, D., & Barry, C. (2018) · Current Biology · doi:10.1016/j.cub.2017.10.073 · Cited by 413 · see citing works
Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D., & Rawlins, J. N. P. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.6.1170 · Cited by 397 · see citing works
Eichenbaum, H., Kuperstein, M., Fagan, A., & Nagode, J. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-03-00716.1987 · Cited by 378 · see citing works
The Hippocampus and Memory for “What,” “Where,” and “When”
Ergorul, C., & Eichenbaum, H. (2004) · Learning & Memory · doi:10.1101/lm.73304 · Cited by 294 · see citing works
Huang, Y.-Y., Kandel, E. R., Varshavsky, L., Brandont, E. P., Qi, M., Idzerda, R. L., Stanley McKnight, G., & Bourtchouladz, R. (1995) · Cell · doi:10.1016/0092-8674(95)90146-9 · Cited by 267 · see citing works
Yamada, K., Tanaka, T., Han, D., Senzaki, K., Kameyama, T., & Nabeshima, T. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00408.x · Cited by 238 · see citing works
Is the avian hippocampus a functional homologue of the mammalian hippocampus?
Colombo, M., & Broadbent, N. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00016-6 · Cited by 237 · see citing works
Chan, C.-S., Weeber, E. J., Zong, L., Fuchs, E., Sweatt, J. D., & Davis, R. L. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4110-05.2006 · Cited by 165 · see citing works
Winocur, G., Moscovitch, M., Fogel, S., Rosenbaum, R. S., & Sekeres, M. (2005) · Nature Neuroscience · doi:10.1038/nn1401 · Cited by 161 · see citing works
Knierim, J. J., & Hamilton, D. A. (2011) · Physiological Reviews · doi:10.1152/physrev.00021.2010 · Cited by 148 · see citing works
Models of anxiety: Responses of rats to novelty in an open space and an enclosed space
Ennaceur, A., Michalikova, S., & Chazot, P. L. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.03.016 · Cited by 117 · see citing works
The development of spatial and memory circuits in the rat
Tan, H. M., Wills, T. J., & Cacucci, F. (2017) · WIREs Cognitive Science · doi:10.1002/wcs.1424 · Cited by 113 · see citing works
Hyde, L. A., Frisone, D. F., & Crnic, L. S. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00313-2 · Cited by 108 · see citing works
Hippocampal Remapping and Its Entorhinal Origin
Latuske, P., Kornienko, O., Kohler, L., & Allen, K. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00253 · Cited by 102 · see citing works
Neurophysiology of Remembering
Buzsáki, G., McKenzie, S., & Davachi, L. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-021721-110002 · Cited by 84 · see citing works
Prema, A., Justin Thenmozhi, A., Manivasagam, T., Mohamed Essa, M., & Guillemin, G. J. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161103 · Cited by 90 · see citing works
Blokland, A., Honig, W., & Raaijmakers, W. G. M. (1992) · Psychopharmacology · doi:10.1007/bf02245886 · Cited by 85 · see citing works
Muhia, M., Yee, B. K., Feldon, J., Markopoulos, F., & Knuesel, I. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07079.x · Cited by 71 · see citing works
Fukuda, E., Hamada, S., Hasegawa, S., Katori, S., Sanbo, M., Miyakawa, T., Yamamoto, T., Yamamoto, H., Hirabayashi, T., & Yagi, T. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06428.x · Cited by 64 · see citing works
Winocur, G., Moscovitch, M., Rosenbaum, R. S., & Sekeres, M. (2010) · Hippocampus · doi:10.1002/hipo.20721 · Cited by 49 · see citing works
Herdman, K. A., Calarco, N., Moscovitch, M., Hirshhorn, M., & Rosenbaum, R. S. (2015) · Cortex · doi:10.1016/j.cortex.2015.06.008 · Cited by 46 · see citing works
Working memory and multidimensional schizotypy: Dissociable influences of the different dimensions
Schmidt-Hansen, M., & Honey, R. C. (2009) · Cognitive Neuropsychology · doi:10.1080/02643291003644501 · Cited by 46 · see citing works
Gökçek-Saraç, Ç., Wesierska, M., & Jakubowska-Doğru, E. (2015) · Learning & Behavior · doi:10.3758/s13420-014-0163-9 · Cited by 28 · see citing works
Manns, J. R., & Eichenbaum, H. (2007) · Evolution of Nervous Systems · doi:10.1016/b0-12-370878-8/00086-0 · Cited by 28 · see citing works
Hauber, W., & Schmidt, W. J. (1989) · Journal of Neural Transmission · doi:10.1007/bf01247111 · Cited by 26 · see citing works
- Authors
- Olton, D. S., Becker, J. T., & Handelmann, G. E.
- Affiliations
- Johns Hopkins University (US)
- ORCID
- Becker, James T.
- Venue
- Behavioral and Brain Sciences
- Publisher
- Cambridge University Press (CUP)
- Published
- 1979-09
- Volume
- 2
- Issue
- 3
- Pages
- 313-322
- ISSN
- 0140-525X (ISSN-L)
- 1469-1825
- OpenAlex
- W2033319161
- Cited by
- 2,018
- References
- 4
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 35 · 2023: 7 · 2022: 15 · 2021: 17 · 2020: 13 · 2019: 11 · 2018: 13 · 2017: 16 · 2016: 19 · 2015: 22 · 2014: 21 · 2013: 30 · 2012: 29
- FWCI
- 34.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral and Brain Sciences (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Keywords
- hippocampus, working memory, reference memory, spatial memory, cognitive maps, hippocampal lesions, rats, spatial behavior
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review