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Neuronal activity in the hippocampus during delayed non‐match to sample performance in rats: Evidence for hippocampal processing in recognition memory
Abstract
Neuronal activity in the CA1 of rats was explored with regard to functional correlates of performance in an odor‐guided continuous delayed non‐match to sample task. Although different CA1 cells fired in association with each identifiable trial event, these analyses focused on cells that fired selectively during the period of odor cue sampling and response generation. The firing patterns of many of these cells reflected the match or non‐match comparison between current and previous odor cues independent of the particular stimuli that composed those comparisons. Such cells were more prevalent in sessions when performance was highly accurate. Hippocampal cells did not demonstrate stimulus‐evoked firing that persisted through the memory delay, nor did they fire differentially to session‐novel vs. repeated odor presentations. These results suggest that the hippocampus contributes to recognition memory by processing comparisons between current information and representations of previous stimuli stored in parahippocampal and neocortical structures.
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“evidence suggests that place cell activity in rats can also encode information about the ‘what’ (e.g. odours and their status, i.e. match/non-match [124–126]) and ‘when’ (i.e. elapsed time [127,128]) of events.”
From Is episodic-like memory like episodic memory? (2024) · cites this paper as [124]
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“More recently, D(N)MS has been run in much the same way, but with computer-graphic stimuli presented on touchscreen monitors (e.g., Ogura and Aigner, 1993; Parker et al., 1997; Parker and Gaffan, 1998).”
Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects
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“In addition, it included the suppression of inhibitory synaptic transmission (1 - xH+) (Pitler and Alger, 1992), the enhancement of excitatory synaptic modification (Burgard and Sarvey, 1990; Huerta and Lisman, 1993), the direct depolarization of inhibitory and excitatory neurons (Benardo and…”
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BackgroundTowards a functional organization of episodic memory in the medial temporal lobe
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BackgroundSelf-citationMemory Representation within the Parahippocampal Region
Young, B. J., Otto, T., Fox, G. D., & Eichenbaum, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05183.1997 · Cited by 372
“In the most directly comparable study, Otto and Eichenbaum (1992b) recorded the activity of CA1 neurons from rats performing the same odor-guided cDNMS task used here.”
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Self-citationRecognition memory: neuronal substrates of the judgement of prior occurrence
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“However, neurons do show short periods of high frequency activity around 30–40 Hz [101,137], and the tendency of excitatory neurons to fire tight clusters of 3–4 action potentials (‘complex spikes’) could form the basis for a rapid approach to an attractor state within one gamma oscillation, partly driven by the intri…”
BackgroundMethodAn Unexpected Sequence of Events: Mismatch Detection in the Human Hippocampus
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The rodent hippocampus is essential for nonspatial object memory
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“Postsurgicalspatial cues, such as odors (Otto and Eichenbaum, 1992; analgesics (2 mg/kg ketoprofen) were given daily for 3 days afterWiebe and Staubli, 1999; Wood et al., 1999) and auditory surgery.tones (Berger et al., 1976; McEchron and Disterhoft, 1997; Munera et al., 2001; Sakurai, 1994), as…”
BackgroundMedial Temporal Lobe Activity Predicts Successful Relational Memory Binding
Hannula, D. E., & Ranganath, C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3086-07.2008 · Cited by 304
Tracking the emergence of conceptual knowledge during human decision making
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“, match versus nonmatch [Hampton et al., 2006; Miller et al., 2002; Otto and Eichenbaum, 1992]), and the integration of social and reward information (Behrens et al.”
The complementary brain: unifying brain dynamics and modularity
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Neural Substrates of Overgeneralized Conditioned Fear in PTSD
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“…these animal and human findings support a neural model of classically conditioned fear generalization (Lissek, 2012) in which CSþ and GS representations in sensory cortex undergo ‘schematic matching’, or same–different assessment by the hippocampus (Otto and Eichenbaum, 1992; Sander et al., 2005).”
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Stern, C. E., Sherman, S. J., Kirchhoff, B. A., & Hasselmo, M. E. (2001) · Hippocampus · doi:10.1002/hipo.1048 · Cited by 249
“The data are also consistent with the finding that prefrontal lesions in the rat cause impairments on DNMS with a small set of 8 odors, but not with a larger set of 16 odors (Otto and Eichenbaum, 1992a).”
BackgroundResultInfluentialPattern separation, pattern completion, and new neuronal codes within a continuous CA3 map
Leutgeb, S., & Leutgeb, J. K. (2007) · Learning & Memory · doi:10.1101/lm.703907 · Cited by 234
“…path to a goal, remapping should at least partially preserve information about places and, in particular, about relevant locations within the spatial coordinate system, such as choice points and goal locations (e.g., Eichenbaum et al. 1987; Otto and Eichenbaum 1992; Fyhn et al. 2002; Knierim 2004).”
Hippocampus, theta, and spatial memory
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Cannabinoids, hippocampal function and memory
Hampson, R. E., & Deadwyler, S. A. (1999) · Life Sciences · doi:10.1016/s0024-3205(99)00294-5 · Cited by 227
Medial prefrontal activity during delay period contributes to learning of a working memory task
Liu, D., Gu, X., Zhu, J., Zhang, X., Han, Z., Yan, W., Cheng, Q., Hao, J., Fan, H., Hou, R., et al. (2014) · Science · doi:10.1126/science.1256573 · Cited by 213
Eichenbaum, H., & Lipton, P. A. (2008) · Hippocampus · doi:10.1002/hipo.20500 · Cited by 222
Self-citationIs the rodent hippocampus just for ‘place’?
Eichenbaum, H. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80072-9 · Cited by 209
Self-citationHippocampus as a memory map: Synaptic plasticity and memory encoding by hippocampal neurons
Shapiro, M. L., & Eichenbaum, H. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 209
Changes in Brain MicroRNAs Contribute to Cholinergic Stress Reactions
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BackgroundShort-term reverberant memory model of hippocampal field CA3
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“This is a robust phenomenon that we and others have previously observed after exposure to a variety of novel experiences (Chowdhury et al. 2000; Fevurly and Spencer 2004; Pace et al. 2005).”
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Self-citationMotivational states activate distinct hippocampal representations to guide goal-directed behaviors
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The Hippocampal System and Declarative Memory in Animals
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Self-citationSpatially selective firing properties of hippocampal formation neurons in rodents and primates
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Spikes, synchrony, and attentive learning by laminar thalamocortical circuits
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Task-Dependent Representations in Rat Hippocampal Place Neurons
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Gilbert, P. E., & Kesner, R. P. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1385 · Cited by 153
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Self-citationThe neurobiology of human fear generalization: meta-analysis and working neural model
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“Given that anterior insula has been linked to interoceptive awareness of the somatic correlates of fear (LeDoux and Pine, 2016; Paulus and Stein, 2006; Zaki et al., 2012), positive generalization effects in AI may reflect graded increases in conscious awareness that one’s body is in an anxious…”
Young, B., Fox, G., & Eichenbaum, H. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06553.1994 · Cited by 142
“…striking nonspatial correlates of hippocampal unit activity have been observed in a variety of formal learning paradigms where spatial cues are minimized or made irrelevant (Berger et al., 1983; Wible et al., 1986; Eichenbaum et al., 1987; Wiener et al., 1989; Otto and Eichenbaum, 1992).”
BackgroundInfluentialSelf-citationNeural dynamics of autistic behaviors: Cognitive, emotional, and timing substrates.
Grossberg, S., & Seidman, D. (2006) · Psychological Review · doi:10.1037/0033-295x.113.3.483 · Cited by 142
“…of learned categories in (say) the inferotemporal cortex (Spitzer et al., 1988) and the number of novelty-triggered N200 potentials (Deadwyler et al., 1979, Deadwyler et al., 1981) or even novelty-sensitive cells (Otto and Eichenbaum, 1992) in the hippocampus (Carpenter and Grossberg, 1993).”
BackgroundThe Hippocampus and Cerebellum in Adaptively Timed Learning, Recognition, and Movement
Grossberg, S., & Merrill, J. W. L. (1996) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1996.8.3.257 · Cited by 137
“In particular, the novelty-sensitive matching and memory search properties that are modulated by the ART orienting subsystem suggest how the hippocampal system may contribute to exible expression of memories in novel contexts and why hippocampal neurons respond di erently to match and non-match conditions (Otto and Ei…”
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Sakurai, Y. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02606.1994 · Cited by 126
“…are consistent with the result ofa previous study (Sakurai, 1990a) that showed CA 1 and CA3 involvement in comparisons for WM, and are supported by several other studies (Gabriel et al., 1986; Gray and Rawlins, 1986; Eichenbaum et al., 1987; Foster et al., 1987; Otto and Eichenbaum, 1992).”
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Neural Correlates of Olfactory Recognition Memory in the Rat Orbitofrontal Cortex
Ramus, S. J., & Eichenbaum, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08199.2000 · Cited by 120
Self-citationGrossberg, S. (2017) · Neural Networks · doi:10.1016/j.neunet.2016.11.003 · Cited by 120
Differential but Complementary Mnemonic Functions of the Hippocampus and Subiculum
Deadwyler, S. A., & Hampson, R. E. (2004) · Neuron · doi:10.1016/s0896-6273(04)00195-3 · Cited by 123
“Since hip- 1993; Wiener et al., 1989; Otto and Eichenbaum, 1992).”
BackgroundNeurobiological Views of Memory
Kesner, R. P. (1998) · Elsevier eBooks · doi:10.1016/b978-012475655-7/50011-3 · Cited by 121
Role of Cannabinoid Receptors in Memory Storage
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Hampson, R. E., Rogers, G. A., LYNCH, G. S., & Deadwyler, S. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-07-02748.1998 · Cited by 117
“Extensive electrophysiological investigations in rodents and monkeys show that hippocampal neurons are “engaged” during “delay”-type memory tasks (Cahusac et al., 1989; Miller et al., 1991, 1996; Otto and Eichenbaum, 1992; Hampson et al., 1993; Rolls et al., 1993; Colombo and Gross, 1994).”
BackgroundHuman Hippocampal Neurons Predict How Well Word Pairs Will Be Remembered
Cameron, K. A., Yashar, S., Wilson, C. L., & Fried, I. (2001) · Neuron · doi:10.1016/s0896-6273(01)00280-x · Cited by 113
Doyère, V., Burette, F., Negro, C. D., & Laroche, S. (1993) · Neuropsychologia · doi:10.1016/0028-3932(93)90031-t · Cited by 115
The effects of perirhinal cortical lesions on spatial reference memory in the rat
Wiig, K. A., & Bilkey, D. K. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90055-8 · Cited by 110
Recognition memory in rats—II. Neuroanatomical substrates
Steckler, T., Drinkenburg, W. H. I. M., Sahgal, A., & Aggleton, J. P. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00061-0 · Cited by 108
Wirt, R. A., & Hyman, J. M. (2017) · Brain Sciences · doi:10.3390/brainsci7040043 · Cited by 109
“The first characterization suggests that mPFC activity should be rather similar to hippocampal activity, and in some cases that are thought to be strongly related to memory processing, this is true; for example, neurons in both areas exhibit strong stimulus and response behavioral correlates [141,142]; exhibit theta p…”
BackgroundA unified model of spatial and episodic memory
Rolls, E. T., Stringer, S. M., & Trappenberg, T. P. (2002) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2009 · Cited by 97
“…a conditional spatial response task where the behavioural response depends on the object shown (Miyashita et al. 1989), and in that in the rat some neurons respond to non-spatial information in memory tasks (Wiener et al. 1989; Otto & Eichenbaum 1992; Hampson et al. 1999; Eichenbaum & Harris 2000).”
BackgroundJohnson, A. C., & Redish, A. D. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.009 · Cited by 92
“Similarly, hippocampal cells are sensitive to match and non-match of samples when animals were forced to make a decision based on that match versus non-match (Cohen & Eichenbaum, 1993; Otto & Eichenbaum, 1992; Sakurai, 1990).”
Vago, D. R., & Kesner, R. P. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.01.002 · Cited by 100
The hippocampal debate: are we asking the right questions?
Redish, A. D. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00356-4 · Cited by 87
“It is the contention of this paper that the sensitivity to non-spatial stimuli, as well as to cue-conflict, can also be explained by postulating a role of the hippocampus in associating external cues with internal representations, not of location on a cognitivemap, but rather of different maps.”
BackgroundDynamic Filtering of Recognition Memory Codes in the Hippocampus
Wiebe, S. P., & Staubli, U. V. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10562.1999 · Cited by 88
“This agrees with previous findings from the CA3 and CA1 fields ( Otto and Eichenbaum, 1992b; Hampson et al., 1993), but now extends them into dentate granule cells.”
BackgroundResultInfluentialComplementary Roles of Hippocampus and Medial Entorhinal Cortex in Episodic Memory
Lipton, P. A., & Eichenbaum, H. (2008) · Neural Plasticity · doi:10.1155/2008/258467 · Cited by 95
“In addition, hippocampal neuronal activity has been associated with a variety of nonspatial cues, behaviors, and task demands [16–27], consistent with additional findings showing a critical role for the hippocampus in nonspatial as well as spatial learning and memory [28– 30].”
Self-citationHampson, R. E., Byrd, D. R., Konstantopoulos, J. K., Bunn, T., & Deadwyler, S. A. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:3 · Cited by 82
Soya isoflavone supplementation enhances spatial working memory in men
Thorp, A. A., Parletta, N., Buckley, J. D., Coates, A. M., & Howe, P. R. C. (2009) · British Journal Of Nutrition · doi:10.1017/s0007114509990201 · Cited by 77
Petrulis, A., Alvarez, P., & Eichenbaum, H. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.09.001 · Cited by 75
“This hypothesis is supported by the finding that damage to the perirhinal‐entorhinal cortex (Prh-Ent), which produces impairments in performance on spontaneous object recognition and visual- and olfactory-guided delayed non-matchto-sample (DNMTS) tasks (Brown and Aggleton, 2001; Mumby, 2001; Otto and Eichenbaum, 1992…”
ResultSelf-citationRecognition Memory Correlates of Hippocampal Theta Cells
Wiebe, S. P., & Staubli, U. V. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-03955.2001 · Cited by 75
“Hippocampal principal cells are known to encode both odors (Wiebe and Stäubli, 1999; Wood et al., 1999) and match / nonmatch comparisons (Otto and Eichenbaum, 1992; Rolls et al., 1993; Deadwyler et al., 1996; Wood et al., 1999) within the DNMS recognition memory task.”
BackgroundInfluentialYoung, B. J., & McNaughton, N. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-18-07043.2000 · Cited by 69
“An alternative and, in the case of the present data, more plausible account of the function of the cells in Figure 3 is that their decrementing activity reflects a decaying memory trace of the previous response, and as such, may be similar to the hippocampal “delay cells” described previously in both rats ( Otto and E…”
ResultGelinas, J. N., Tenorio, G., Lemon, N., Abel, T. G., & Nguyen, P. (2008) · Learning & Memory · doi:10.1101/lm.829208 · Cited by 71
“Field potential oscillations in the range of 3–12 Hz are observed in the hippocampus in vivo (Otto et al. 1991; Stewart et al. 1992).”
BackgroundGrossberg, S. (2007) · Neural Networks · doi:10.1016/j.neunet.2007.09.014 · Cited by 67
Role of the hippocampal formation in learning and memory
Jaffard, R., & Meunier, M. (1993) · Hippocampus · doi:10.1002/hipo.1993.4500030724 · Cited by 76
de Araújo, I. E., Rolls, E. T., & Stringer, S. M. (2001) · Hippocampus · doi:10.1002/hipo.1085 · Cited by 67
“The finding that some rat hippocampal neurons reflect more than the place where the rat is located is consistent with the possibility that rat hippocampal neurons are involved in a memory process (Wiener et al., 1989; Otto and Eichenbaum, 1992; Hampson et al., 1999; Eichenbaum and Harris, 2000; Kali and Dayan, 2000) (…”
BackgroundResultWeak and Nondiscriminative Responses to Conspecifics in the Rat Hippocampus
von Heimendahl, M., Rao, R. P., & Brecht, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3812-11.2012 · Cited by 66
“While animals were performing olfactory (Eichenbaum et al., 1987; Otto and Eichenbaum, 1992; Wood et al., 1999; Wiebe and Stäubli, 2001; Deshmukh and Bhalla, 2003; Komorowski et al., 2009), auditory (Sakurai, 1994; Moita et al., 2003), visual (Wible et al., 1986), tactile (Pereira et al., 2007;…”
BackgroundComputational Modeling of Entorhinal Cortex
Hasselmo, M. E., Fransén, E. A., Dickson, C. T., & Alonso, A. A. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06741.x · Cited by 63
“136,137,67 This match enhancement could reduce modulatory input from the medial septum to put the network into more of a “retrieval” state when there is a consistent match between retrieval and afferent input.”
BackgroundWiener, S. I., Berthoz, A., & Zugaro, M. (2002) · Cognitive Brain Research · doi:10.1016/s0926-6410(02)00062-9 · Cited by 60
“cy that has been replicated in odor discrimination tasks These dramatic context-related changes in discharge corre- [15,76].”
BackgroundKnauer, B., Jochems, A., Valero-Aracama, M. J., & Yoshida, M. (2013) · Hippocampus · doi:10.1002/hipo.22136 · Cited by 67
“Cholinergic receptor activation is also known to enhance synaptic plasticity (Huerta and Lisman, 1993; Ovsepian et al., 2004; Sugisaki et al., 2011).”
BackgroundMoving beyond standard procedures to assess spontaneous recognition memory
Ameen‐Ali, K. E., Easton, A., & Eacott, M. J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.03.013 · Cited by 63
Differential encoding of place value between the dorsal and intermediate hippocampus
Jin, S., & Lee, I. (2021) · Current Biology · doi:10.1016/j.cub.2021.04.073 · Cited by 56
Anterior medial temporal lobe in human cognition: Memory for fear and the unexpected
Strange, B. A., & Dolan, R. J. (2006) · Cognitive Neuropsychiatry · doi:10.1080/13546800500305096 · Cited by 60
Lithium treatment alleviates impaired cognition in a mouse model of fragile X syndrome
King, M. K., & Jope, R. S. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12071 · Cited by 59
“Recently, severe deficits in nonaversive learning and memory tasks, including novel object recognition and context discrimination, have been identified in Fmr1 KO mice (Bhattacharya & Klann 2012; Eadie et al. 2012; Pacey et al. 2011).”
BackgroundBannerman, D. M., Lemaire, M., Yee, B. K., Iversen, S. D., Oswald, C., Good, M. A., & Rawlins, J. N. P. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0938-z · Cited by 57
“These data are in marked contrast to unit recording studies conducted in the hippocampus during the same behavioural task, in which no such cell activity was observed ( Otto and Eichenbaum 1992b ).”
Dudukovic, N. M., Preston, A. R., Archie, J. J., Glover, G. H., & Wagner, A. D. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21509 · Cited by 56
Sarter, M. F., Bruno, J. P., Givens, B. S., Moore, H. M., McGaughy, J. A., & McMahon, K. (1996) · Cognitive Brain Research · doi:10.1016/0926-6410(96)00018-3 · Cited by 55
The mysteries of remote memory
Albo, Z., & Gräff, J. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0029 · Cited by 55
Auditory Spatial Discriminatory and Mnemonic Neurons in Rat Posterior Parietal Cortex
Nakamura, K. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.5.2503 · Cited by 54
“The medial temporal memory consolidation system is known to be activated by unfamiliar stimuli (Cahusac et al. 1989; Miyashita et al. 1989; Otto and Eichenbaum 1992; Rolls et al. 1989).”
BackgroundInfluentialThe hippocampus: Relational processor or antiprocessor?
McNaughton, N. (1994) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00035561 · Cited by 52
Ramus, S. J., DAVIS, J. B., Donahue, R. J., Discenza, C. B., & WAITE, A. A. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1401.038 · Cited by 54
Newmark, R. E., Schön, K., Ross, R. S., & Stern, C. E. (2013) · Hippocampus · doi:10.1002/hipo.22106 · Cited by 50
Tsanov, M., & Manahan-Vaughan, D. (2008) · The Neuroscientist · doi:10.1177/1073858408315655 · Cited by 65
“It also plays a role in associating objects with other sensory representations as tactile (Goulet and Murray 2001) and gustatory information with objects (Parker and Gaffan 1998).”
BackgroundVisual perception and memory systems: from cortex to medial temporal lobe
Khan, Z. U., Martín‐Montañez, E., & Baxter, M. G. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0641-6 · Cited by 53
Metadata
- Authors
- Otto, T., & Eichenbaum, H.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Otto, Tim
- ORCID
- Eichenbaum, Howard
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 1992-07
- Volume
- 2
- Issue
- 3
- Pages
- 323-334
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2117977220
- Cited by
- 232
- References
- 58
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 4 · 2018: 7 · 2017: 5 · 2016: 5 · 2015: 5 · 2014: 7 · 2013: 8 · 2012: 5
- FWCI
- 9.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National Institutes of Health (7r01ns026402-04)
- National Institute on Aging (NIA AG09973)
- National Institute of Neurological Disorders and Stroke (NS26402)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal CA1, neuronal firing patterns, recognition memory, odor-guided behavior, memory comparison
- MeSH terms
- Animals, Evoked Potentials, Hippocampus, Male, Memory, Neurons, Odorants, Psychomotor Performance, Pyramidal Tracts, Reward, Time Factors, Rats
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