The Journal of Neurophysiology Vol. 78 No. 2 August 1997, pp. 1062-1081
Copyright ©1997 The American Physiological Society

Object and Place Memory in the Macaque Entorhinal Cortex

Wendy A. Suzuki¹, Earl K. Miller², and Robert Desimone¹

¹ Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892-4415; and ² Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Suzuki, Wendy A., Earl K. Miller, and Robert Desimone. Object and place memory in the macaque entorhinal cortex. J. Neurophysiol. 78: 1062-1081, 1997. Lesions of the entorhinal cortex in humans, monkeys, and rats impair memory for a variety of kinds of information, including memory for objects and places. To begin to understand the contribution of entorhinal cells to different forms of memory, responses of entorhinal cells were recorded as monkeys performed either an object or place memory task. The object memory task was a variation of delayed matching to sample. A sample picture was presented at the start of the trial, followed by a variable sequence of zero to four test pictures, ending with a repetition of the sample (i.e., a match). The place memory task was a variation of delayed matching to place. In this task, a cue stimulus was presented at a variable sequence of one to four "places" on a computer screen, ending with a repetition of one of the previously shown places (i.e., a match). For both tasks, the animals were rewarded for releasing a bar to the match. To solve these tasks, the monkey must 1) discriminate the stimuli, 2) maintain a memory of the appropriate stimuli during the course of the trial, and 3) evaluate whether a test stimulus matches previously presented stimuli. The responses of entorhinal cortex neurons were consistent with a role in all three of these processes in both tasks. We found that 47% and 55% of the visually responsive entorhinal cells responded selectively to the different objects or places presented during the object or place task, respectively. Similar to previous findings in prefrontal but not perirhinal cortex on the object task, some entorhinal cells had sample-specific delay activity that was maintained throughout all of the delay intervals in the sequence. For the place task, some cells had location-specific maintained activity in the delay immediately following a specific cue location. In addition, 59% and 22% of the visually responsive cells recorded during the object and place task, respectively, responded differently to the test stimuli according to whether they were matching or nonmatching to the stimuli held in memory. Responses of some cells were enhanced to matching stimuli, whereas others were suppressed. This suppression or enhancement typically occurred well before the animals' behavioral response, suggesting that this information could be used to perform the task. These results indicate that entorhinal cells receive sensory information about both objects and spatial locations and that their activity carries information about objects and locations held in short-term memory.

This article has been cited by other articles:

				P. S.F. Bellgowan, E. A. Buffalo, J. Bodurka, and A. Martin Lateralized spatial and object memory encoding in entorhinal and perirhinal cortices Learn. Mem., June 24, 2009; 16(7): 433 - 438. [Abstract] [Full Text] [PDF]

				L. Woloszyn and D. L. Sheinberg Neural Dynamics in Inferior Temporal Cortex during a Visual Working Memory Task J. Neurosci., April 29, 2009; 29(17): 5494 - 5507. [Abstract] [Full Text] [PDF]

				K. Schon, Y. T. Quiroz, M. E. Hasselmo, and C. E. Stern Greater Working Memory Load Results in Greater Medial Temporal Activity at Retrieval Cereb Cortex, February 18, 2009; (2009) bhp006v1. [Abstract] [Full Text] [PDF]

				N. Axmacher, C. E. Elger, and J. Fell Working Memory-Related Hippocampal Deactivation Interferes with Long-Term Memory Formation J. Neurosci., January 28, 2009; 29(4): 1052 - 1060. [Abstract] [Full Text] [PDF]

				A. H. Lara, S. W. Kennerley, and J. D. Wallis Encoding of Gustatory Working Memory by Orbitofrontal Neurons J. Neurosci., January 21, 2009; 29(3): 765 - 774. [Abstract] [Full Text] [PDF]

				K. Duncan, C. Curtis, and L. Davachi Distinct Memory Signatures in the Hippocampus: Intentional States Distinguish Match and Mismatch Enhancement Signals J. Neurosci., January 7, 2009; 29(1): 131 - 139. [Abstract] [Full Text] [PDF]

				M. Tsanov and D. Manahan-Vaughan Synaptic Plasticity from Visual Cortex to Hippocampus: Systems Integration in Spatial Information Processing Neuroscientist, December 1, 2008; 14(6): 584 - 597. [Abstract] [PDF]

				N. Axmacher, D. P. Schmitz, I. Weinreich, C. E. Elger, and J. Fell Interaction of Working Memory and Long-Term Memory in the Medial Temporal Lobe Cereb Cortex, December 1, 2008; 18(12): 2868 - 2878. [Abstract] [Full Text] [PDF]

				F. Mormann, S. Kornblith, R. Q. Quiroga, A. Kraskov, M. Cerf, I. Fried, and C. Koch Latency and Selectivity of Single Neurons Indicate Hierarchical Processing in the Human Medial Temporal Lobe J. Neurosci., September 3, 2008; 28(36): 8865 - 8872. [Abstract] [Full Text] [PDF]

				I. Lee and F. Solivan The roles of the medial prefrontal cortex and hippocampus in a spatial paired-association task Learn. Mem., May 5, 2008; 15(5): 357 - 367. [Abstract] [Full Text] [PDF]

				B. Tahvildari, A. A. Alonso, and C. W. Bourque Ionic Basis of ON and OFF Persistent Activity in Layer III Lateral Entorhinal Cortical Principal Neurons J Neurophysiol, April 1, 2008; 99(4): 2006 - 2011. [Abstract] [Full Text] [PDF]

				D. E. Hannula and C. Ranganath Medial Temporal Lobe Activity Predicts Successful Relational Memory Binding J. Neurosci., January 2, 2008; 28(1): 116 - 124. [Abstract] [Full Text] [PDF]

				M. Yoshida and A. Alonso Cell-Type Specific Modulation of Intrinsic Firing Properties and Subthreshold Membrane Oscillations by the M(Kv7)-Current in Neurons of the Entorhinal Cortex J Neurophysiol, November 1, 2007; 98(5): 2779 - 2794. [Abstract] [Full Text] [PDF]

				I. Dinstein, U. Hasson, N. Rubin, and D. J. Heeger Brain Areas Selective for Both Observed and Executed Movements J Neurophysiol, September 1, 2007; 98(3): 1415 - 1427. [Abstract] [Full Text] [PDF]

				R. A. Koene and M. E. Hasselmo First-In-First-Out Item Replacement in a Model of Short-Term Memory Based on Persistent Spiking Cereb Cortex, August 1, 2007; 17(8): 1766 - 1781. [Abstract] [Full Text] [PDF]

				N. Axmacher, F. Mormann, G. Fernandez, M. X Cohen, C. E. Elger, and J. Fell Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe J. Neurosci., July 18, 2007; 27(29): 7807 - 7816. [Abstract] [Full Text] [PDF]

				J. J. Knierim Neural representations of location outside the hippocampus Learn. Mem., July 1, 2006; 13(4): 405 - 415. [Abstract] [Full Text] [PDF]

				I. R. Olson, K. Page, K. S. Moore, A. Chatterjee, and M. Verfaellie Working memory for conjunctions relies on the medial temporal lobe. J. Neurosci., April 26, 2006; 26(17): 4596 - 4601. [Abstract] [Full Text] [PDF]

				G. Schoenbaum, B. Setlow, M. P. Saddoris, and M. Gallagher Encoding Changes in Orbitofrontal Cortex in Reversal-Impaired Aged Rats J Neurophysiol, March 1, 2006; 95(3): 1509 - 1517. [Abstract] [Full Text] [PDF]

				D. Yoganarasimha, X. Yu, and J. J. Knierim Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells J. Neurosci., January 11, 2006; 26(2): 622 - 631. [Abstract] [Full Text] [PDF]

				K. Schon, A. Atri, M. E. Hasselmo, M. D. Tricarico, M. L. LoPresti, and C. E. Stern Scopolamine Reduces Persistent Activity Related to Long-Term Encoding in the Parahippocampal Gyrus during Delayed Matching in Humans J. Neurosci., October 5, 2005; 25(40): 9112 - 9123. [Abstract] [Full Text] [PDF]

				E. L. Hargreaves, G. Rao, I. Lee, and J. J. Knierim Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus Science, June 17, 2005; 308(5729): 1792 - 1794. [Abstract] [Full Text] [PDF]

				W. A. Suzuki and E. N. Brown Behavioral and Neurophysiological Analyses of Dynamic Learning Processes Behav Cogn Neurosci Rev, June 1, 2005; 4(2): 67 - 95. [Abstract] [PDF]

				L. M. Talamini, M. Meeter, B. Elvevag, J. M. J. Murre, and T. E. Goldberg Reduced Parahippocampal Connectivity Produces Schizophrenia-like Memory Deficits in Simulated Neural Circuits With Reduced Parahippocampal Connectivity Arch Gen Psychiatry, May 1, 2005; 62(5): 485 - 493. [Abstract] [Full Text] [PDF]

				T. Sommer, M. Rose, J. Glascher, T. Wolbers, and C. Buchel Dissociable contributions within the medial temporal lobe to encoding of object-location associations Learn. Mem., May 1, 2005; 12(3): 343 - 351. [Abstract] [Full Text] [PDF]

				K. Schon, M. E. Hasselmo, M. L. LoPresti, M. D. Tricarico, and C. E. Stern Persistence of Parahippocampal Representation in the Absence of Stimulus Input Enhances Long-Term Encoding: A Functional Magnetic Resonance Imaging Study of Subsequent Memory after a Delayed Match-to-Sample Task J. Neurosci., December 8, 2004; 24(49): 11088 - 11097. [Abstract] [Full Text] [PDF]

				C. Constantinidis and X.-J. Wang A Neural Circuit Basis for Spatial Working Memory Neuroscientist, December 1, 2004; 10(6): 553 - 565. [Abstract] [PDF]

				J. Magistretti, L. Ma, M. H. Shalinsky, W. Lin, R. Klink, and A. Alonso Spike Patterning by Ca2+-Dependent Regulation of a Muscarinic Cation Current in Entorhinal Cortex Layer II Neurons J Neurophysiol, September 1, 2004; 92(3): 1644 - 1657. [Abstract] [Full Text] [PDF]

				J. J. Knierim How to Avoid Going Bump in the Night: Object and Place Representations in the Hippocampus J. Gen. Physiol., June 28, 2004; 124(1): 3 - 6. [Full Text] [PDF]

				R. E. Hampson, T. P. Pons, T. R. Stanford, and S. A. Deadwyler Categorization in the monkey hippocampus: A possible mechanism for encoding information into memory PNAS, March 2, 2004; 101(9): 3184 - 3189. [Abstract] [Full Text] [PDF]

				L. M. Frank, U. T. Eden, V. Solo, M. A. Wilson, and E. N. Brown Contrasting Patterns of Receptive Field Plasticity in the Hippocampus and the Entorhinal Cortex: An Adaptive Filtering Approach J. Neurosci., May 1, 2002; 22(9): 3817 - 3830. [Abstract] [Full Text] [PDF]

				T. Orlov, V. Yakovlev, D. Amit, S. Hochstein, and E. Zohary Serial Memory Strategies in Macaque Monkeys: Behavioral and Theoretical Aspects Cereb Cortex, March 1, 2002; 12(3): 306 - 317. [Abstract] [Full Text] [PDF]

				E. Fransen, A. A. Alonso, and M. E. Hasselmo Simulations of the Role of the Muscarinic-Activated Calcium-Sensitive Nonspecific Cation Current INCM in Entorhinal Neuronal Activity during Delayed Matching Tasks J. Neurosci., February 1, 2002; 22(3): 1081 - 1097. [Abstract] [Full Text] [PDF]

				H. L. O'Brien, S. J. Tetewsky, L. M. Avery, L. A. Cushman, W. Makous, and C. J. Duffy Visual Mechanisms of Spatial Disorientation in Alzheimer's Disease Cereb Cortex, November 1, 2001; 11(11): 1083 - 1092. [Abstract] [Full Text] [PDF]

				T. Kato, D. Knopman, and H. Liu Dissociation of regional activation in mild AD during visual encoding: A functional MRI study Neurology, September 11, 2001; 57(5): 812 - 816. [Abstract] [Full Text] [PDF]

				L. Davachi and P. S. Goldman-Rakic Primate Rhinal Cortex Participates in Both Visual Recognition and Working Memory Tasks: Functional Mapping With 2-DG J Neurophysiol, June 1, 2001; 85(6): 2590 - 2601. [Abstract] [Full Text] [PDF]

				C. J. Ploner, B. M. Gaymard, S. Rivaud-Pechoux, M. Baulac, S. Clemenceau, S. Samson, and C. Pierrot-Deseilligny Lesions Affecting the Parahippocampal Cortex Yield Spatial Memory Deficits in Humans Cereb Cortex, December 1, 2000; 10(12): 1211 - 1216. [Abstract] [Full Text] [PDF]

				J. W. Bisley and T. Pasternak The Multiple Roles of Visual Cortical Areas MT/MST in Remembering the Direction of Visual Motion Cereb Cortex, November 1, 2000; 10(11): 1053 - 1065. [Abstract] [Full Text] [PDF]

				S. J. Ramus and H. Eichenbaum Neural Correlates of Olfactory Recognition Memory in the Rat Orbitofrontal Cortex J. Neurosci., November 1, 2000; 20(21): 8199 - 8208. [Abstract] [Full Text] [PDF]

				S. P. Wiebe and U. V. Staubli Dynamic Filtering of Recognition Memory Codes in the Hippocampus J. Neurosci., December 1, 1999; 19(23): 10562 - 10574. [Abstract] [Full Text] [PDF]

				N. Matsumura, H. Nishijo, R. Tamura, S. Eifuku, S. Endo, and T. Ono Spatial- and Task-Dependent Neuronal Responses during Real and Virtual Translocation in the Monkey Hippocampal Formation J. Neurosci., March 15, 1999; 19(6): 2381 - 2393. [Abstract] [Full Text] [PDF]