Cholinergic Neurotransmission Is Essential for Perirhinal Cortical Plasticity and Recognition Memory
Open accessAbstract
We establish the importance of cholinergic neurotransmission to both recognition memory and plasticity within the perirhinal cortex of the temporal lobe. The muscarinic receptor antagonist scopolamine impaired the preferential exploration of novel over familiar objects, disrupted the normal reduced activation of perirhinal neurones to familiar compared to novel pictures, and blocked production of long-term depression (LTD) but not long-term potentiation (LTP) of synaptic transmission in perirhinal slices. The consistency of these effects across the behavioral, systems, and cellular levels of analysis provides strong evidence for the involvement of cholinergic mechanisms in synaptic plastic processes within perirhinal cortex that are necessary for recognition memory.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
This depression of synaptic efficacy could contribute to the repetition suppression of neural responses in areas such as the perirhinal cortex.
“This depression of synaptic efficacy could contribute to the repetition suppression of neural responses in areas such as the perirhinal cortex (Bogacz and Brown, 2003; Warburton et al., 2003).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Warburton et al., 2003
Muscarinic receptor activation causes long-term depression of synaptic efficacy.
“Muscarinic receptor activation causes long-term depression of synaptic efficacy (Kirkwood et al., 1999; Warburton et al., 2003).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Warburton et al., 2003
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Recognition memory: What are the roles of the perirhinal cortex and hippocampus?
Brown, M. W., & Aggleton, J. P. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049064 · Cited by 1,555 · see citing works
Self-citationHuman Memory and the Cholinergic System
Drachman, D. A. (1974) · Archives of Neurology · doi:10.1001/archneur.1974.00490320001001 · Cited by 1,398 · 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
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,300 · see citing works
Meunier, M., Bachevalier, J., Mishkin, M., & Murray, E. A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05418.1993 · Cited by 900 · see citing works
Bartus, R. T. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7397 · Cited by 829 · see citing works
Neuromodulation: acetylcholine and memory consolidation
Hasselmo, M. E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01365-0 · Cited by 809 · see citing works
Zola-Morgan, S. M., Squire, L., Amaral, D., & Suzuki, W. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04355.1989 · Cited by 766 · see citing works
The Cholinergic Synapse and the Site of Memory
Deutsch, J. A. (1972) · Advances in behavioral biology · doi:10.1007/978-1-4684-3060-8_11 · Cited by 740 · see citing works
The Cholinergic Synapse and the Site of Memory
Deutsch, J. A. (1971) · Science · doi:10.1126/science.174.4011.788 · Cited by 662 · see citing works
Parallel Neuronal Mechanisms for Short-Term Memory
Miller, E. K., & Desimone, R. (1994) · Science · doi:10.1126/science.8290960 · Cited by 630 · see citing works
Acetylcholine: a neurotransmitter for learning and memory?
Blokland, A. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(95)00016-x · Cited by 613 · see citing works
Dix, S. L., & Aggleton, J. P. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00079-5 · Cited by 598 · see citing works
Self-citationNeuromodulation and cortical function: modeling the physiological basis of behavior
Hasselmo, M. E. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00113-t · Cited by 552 · see citing works
Suzuki, W., Zola-Morgan, S. M., Squire, L., & Amaral, D. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02430.1993 · Cited by 543 · see citing works
Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory
Wan, H., Aggleton, J. P., & Brown, M. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-03-01142.1999 · Cited by 449 · see citing works
Self-citationPerceptual–mnemonic functions of the perirhinal cortex
Murray, E. A. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01303-0 · Cited by 441 · see citing works
Inferotemporal Neurons Distinguish and Retain Behaviorally Relevant Features of Visual Stimuli
Fuster, J. M., & Jervey, J. P. (1981) · Science · doi:10.1126/science.7233192 · Cited by 436 · see citing works
Xiang, J. ‐., & Brown, M. W. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00030-6 · Cited by 425 · see citing works
Self-citationAnderson, W. W., & Collingridge, G. L. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(01)00374-0 · Cited by 423 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.11 · Cited by 412 · see citing works
Ennaceur, A., Neave, N., & Aggleton, J. P. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(96)00006-x · Cited by 351 · see citing works
Self-citationRhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.11 · Cited by 348 · see citing works
Otto, T., & Eichenbaum, H. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.5.762 · Cited by 343 · see citing works
Hasselmo, M. E., & Wyble, B. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00048-x · Cited by 337 · see citing works
Recognition memory: neuronal substrates of the judgement of prior occurrence
Brown, M. W., & Xiang, J. ‐. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00002-1 · Cited by 329 · see citing works
Self-citationEffects of Shape-Discrimination Training on the Selectivity of Inferotemporal Cells in Adult Monkeys
Kobatake, E., Wang, G., & Tanaka, K. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.324 · Cited by 329 · see citing works
Otto, T., & Eichenbaum, H. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.5.762 · Cited by 317 · see citing works
Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine
Kirkwood, A., Rozas, C., Kirkwood, J., Perez, F., & Bear, M. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01599.1999 · Cited by 315 · see citing works
The role of acetylcholine in cortical synaptic plasticity
Rasmusson, D. D. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00259-x · Cited by 267 · see citing works
Gaffan, D., & Murray, E. A. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.30 · Cited by 265 · see citing works
The effects of physostigmine and scopolamine on recognition memory in monkeys
Aigner, T. G., & Mishkin, M. (1986) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(86)80008-5 · Cited by 220 · see citing works
Gaffan, D., & Murray, E. A. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.1.30 · Cited by 217 · see citing works
Hasselmo, M. E., & Barkai, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06592.1995 · Cited by 215 · see citing works
What have ablation studies told us about the neural substrates of stimulus memory?
Murray, E. A. (1996) · Seminars in Neuroscience · doi:10.1006/smns.1996.0003 · Cited by 213 · see citing works
Zhu, X. O., Brown, M. W., McCabe, B. J., & Aggleton, J. P. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00320-i · Cited by 205 · see citing works
Self-citationMeunier, M., Hadfield, W. S., Bachevalier, J., & Murray, E. A. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.3.1190 · Cited by 176 · see citing works
Muscarinic receptors mediating depression and long‐term potentiation in rat hippocampus.
Auerbach, J. M., & Segal, M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021323 · Cited by 168 · see citing works
Cognitive functions of the basal forebrain cholinergic system in monkeys: memory or attention?
Voytko, M. L. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00143-3 · Cited by 160 · see citing works
A new form of long-term depression in the perirhinal cortex
Cho, K., Kemp, N. M., Noël, J., Aggleton, J. P., Brown, M. W., & Bashir, Z. I. (2000) · Nature Neuroscience · doi:10.1038/72093 · Cited by 143 · see citing works
Self-citationComparison of computational models of familiarity discrimination in the perirhinal cortex
Bogacz, R., & Brown, M. W. (2003) · Hippocampus · doi:10.1002/hipo.10093 · Cited by 134 · cited 1× · see citing works
“…of familiarity discrimiinvolvement of cholinergic mechanisms in synaptic nation establishes that synaptic weakening produces a plastic processes within perirhinal cortex that are nec- major gain in storage capacity over synaptic strengthenessary for recognition memory. ing (Bogacz and Brown, 2003).”
BackgroundSelf-citationLearning-related changes in Fos-like immunoreactivity in the chick forebrain after imprinting.
McCabe, B. J., & Horn, G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.24.11417 · Cited by 131 · see citing works
Brennan, P., Hancock, D. C., & Keverne, E. B. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90095-j · Cited by 129 · see citing works
Effects of muscarinic blockade in perirhinal cortex during visual recognition
Tang, Y., Mishkin, M., & Aigner, T. G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12667 · Cited by 125 · see citing works
Mapping visual recognition memory through expression of the immediate early gene c-fos
Zhu, X.-O., McCabe, B. J., Aggleton, J. P., & Brown, M. W. (1996) · Neuroreport · doi:10.1097/00001756-199607290-00037 · Cited by 112 · see citing works
Self-citationModel of Familiarity Discrimination in the Perirhinal Cortex
Bogacz, R., Brown, M. W., & Giraud-Carrier, C. G. (2001) · Journal of Computational Neuroscience · doi:10.1023/a:1008925909305 · Cited by 100 · see citing works
Self-citationEvidence concerning how neurons of the perirhinal cortex may effect familiarity discrimination
Brown, M. W., & Bashir, Z. I. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1097 · Cited by 100 · see citing works
Self-citationMassey, P. V., Bhabra, G., Cho, K., Brown, M. W., & Bashir, Z. I. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01631.x · Cited by 90 · see citing works
Self-citationPerception and Recognition Memory in Monkeys Following Lesions of Area TE and Perirhinal CortexPreprint
Buffalo, E. A. (2000) · Learning & Memory · doi:10.1101/lm.32100 · Cited by 89 · see citing works
de Lima, A. D., Merten, M. D. P., & Voigt, T. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970602)382:2 · Cited by 80 · see citing works
Albright, T. D., Kandel, E. R., & Posner, M. I. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00132-x · Cited by 69 · see citing works
Cholinergic mechanisms in a simple test of olfactory learning in the rat
Hunter, A. J., & Murray, T. K. (1989) · Psychopharmacology · doi:10.1007/bf00442821 · Cited by 68 · see citing works
Scopolamine affects short-term memory but not inferior temporal neurons
Miller, E. K., & Desimone, R. (1993) · NeuroReport · doi:10.1097/00001756-199301000-00021 · Cited by 66 · cited 7× · see citing works
“This finding supports the impairment of recognition memory finding contrasts with the lack of effect found at short found with perirhinal scopolamine infusion in monkeys (5 s) delays in monkeys ( Miller and Desimone, 1993 ).”
BackgroundResultInfluentialRecognition memory in rats—III. Neurochemical substrates
Steckler, T., Sahgal, A., Aggleton, J. P., & Drinkenburg, W. H. I. M. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00062-2 · Cited by 50 · see citing works
Self-citationNeuronal responses and recognition memory
Brown, M. W. (1996) · Seminars in Neuroscience · doi:10.1006/smns.1996.0004 · Cited by 43 · see citing works
Self-citationThe effects of cholinergic drugs upon recognition memory in rats.
Ae, H., & Aggleton, J. P. (1987) · PubMed · Cited by 31 · see citing works
Self-citationEaston, A., Parker, A. J., & Gaffan, D. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00384-3 · Cited by 30 · see citing works
Nimodipine prevents scopolamine-induced impairments in object recognition
Norman, G., Brooks, S. P., Hennebry, G., et al. (2002) · Journal of Psychopharmacology · doi:10.1177/026988110201600206 · Cited by 20 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Swanson, L.W. (1998). Brain Maps: Structure of the Rat Brain (Ox- Neurosci. 15, 6592-6604. ford: Elsevier).
Cited by
Sorted by citations
Long-term depression in the CNS
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2867 · Cited by 926 · see citing works
Modes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Lüscher, C., & Huber, K. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.016 · Cited by 627 · see citing works
Mechanisms underlying working memory for novel information
Hasselmo, M. E., & Stern, C. E. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.09.005 · Cited by 249 · see citing works
Romberg, C., Yang, S., Melani, R., Andrews, M. R., Horner, A. E., Spillantini, M. G., Bussey, T. J., Fawcett, J. W., Pizzorusso, T., & Saksida, L. M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.6267-11.2013 · Cited by 231 · see citing works
Aggleton, J. P., Brown, M. W., & Albasser, M. M. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.05.018 · Cited by 79 · see citing works
Self-citationKenney, J. W., Adoff, M. D., Wilkinson, D. S., & Gould, T. J. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2283-7 · Cited by 67 · see citing works
Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats
Melichercik, A. M., Elliott, K. S., Bianchi, C., Ernst, S. M., & Winters, B. D. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.008 · Cited by 54 · see citing works
c-Fos expression correlates with performance on novel object and novel place recognition tests
Mendez, M., Arias, N., Uceda, S., & Arias, J. L. (2015) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2015.07.004 · Cited by 54 · see citing works
Muscarinic control of long-range GABAergic inhibition within the rhinal cortices
Apergis-Schoute, J., Pinto, A., & Paré, D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0068-07.2007 · Cited by 46 · see citing works
Dürschmid, S., Reichert, C., Kuhn, J., Freund, H., Hinrichs, H., & Heinze, H. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.13749 · Cited by 31 · see citing works
Balderas, I., Morin, J.-P., Rodriguez-Ortiz, C. J., & Bermudez-Rattoni, F. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.03.006 · Cited by 29 · see citing works
Olarte-Sánchez, C. M., Kinnavane, L., Amin, E., & Aggleton, J. P. (2014) · Behavioral Neuroscience · doi:10.1037/a0037055 · Cited by 18 · see citing works
- Authors
- Warburton, E. C., Koder, T., Cho, K., Massey, P. V., Duguid, G., Barker, G. R. I., Aggleton, J. P., Bashir, Z. I., & Brown, M. W.
- Affiliations
- University of Bristol (GB)
- Corresponding author
- Brown, Malcolm W
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2003-06
- Volume
- 38
- Issue
- 6
- Pages
- 987-996
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2102815754
- Cited by
- 226
- References
- 60
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 3 · 2023: 9 · 2022: 7 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 14 · 2017: 7 · 2016: 12 · 2015: 11 · 2014: 15 · 2013: 12 · 2012: 23
- FWCI
- 4.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- cholinergic neurotransmission, perirhinal cortex, recognition memory, synaptic plasticity, scopolamine, muscarinic receptors, long-term depression, long-term potentiation, object recognition, novel object exploration, temporal lobe
- MeSH terms
- Animals, Male, Memory, Synaptic Transmission, Neuronal Plasticity, Neurons, Receptors, Muscarinic, Scopolamine, Muscarinic Antagonists, Entorhinal Cortex, Recognition, Psychology, Rats
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
