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Inhibitory engrams in perception and memory

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Barron, Helen C., Vogels, Tim P., Behrens, Timothy E., Ramaswami, Mani·2017·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1701812114PMC PMC5495250

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Abstract

Nervous systems use excitatory cell assemblies to encode and represent sensory percepts. Similarly, synaptically connected cell assemblies or “engrams” are thought to represent memories of past experience. Multiple lines of recent evidence indicate that brain systems create and use inhibitory replicas of excitatory representations for important cognitive functions. Such matched “inhibitory engrams” can form through homeostatic potentiation of inhibition onto postsynaptic cells that show increased levels of excitation. Inhibitory engrams can reduce behavioral responses to familiar stimuli, thereby resulting in behavioral habituation. In addition, by preventing inappropriate activation of excitatory memory engrams, inhibitory engrams can make memories quiescent, stored in a latent form that is available for context-relevant activation. In neural networks with balanced excitatory and inhibitory engrams, the release of innate responses and recall of associative memories can occur through focused disinhibition. Understanding mechanisms that regulate the formation and expression of inhibitory engrams in vivo may help not only to explain key features of cognition but also to provide insight into transdiagnostic traits associated with psychiatric conditions such as autism, schizophrenia, and posttraumatic stress disorder.

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Epigenetic Regulations of GABAergic Neurotransmission: Relevance for Neurological Disorders and Epigenetic Therapy
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,951
A cognitive model of posttraumatic stress disorder
Ehlers, A., & Clark, D. M. (2000) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(99)00123-0 · Cited by 6,147
Whatever next? Predictive brains, situated agents, and the future of cognitive science
Clark, A. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12000477 · Cited by 5,924
Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects
Rao, R. P. N., & Ballard, D. H. (1999) · Nature Neuroscience · doi:10.1038/4580 · Cited by 5,483 · cited 1×
“…created by local EI balancing mechanisms, the framework we propose also naturally accommodates inhibitory representations constructed through potential alternative mechanisms (Clark, 2013; Cooke et al., 2015; Kogo and Trengove, 2015; Ramaswami, 2014; Rao and Ballard, 1999; Wacongne et al., 2012).”
Background
The Organization of Behavior; A Neuropsychological Theory.
Attneave, F., B., M., & Hebb, D. O. (1950) · The American Journal of Psychology · doi:10.2307/1418888 · Cited by 5,146
The Organization of Behavior: A Neuropsychological Theory
(1950) · JAMA · doi:10.1001/jama.1950.02910470083028 · Cited by 4,272
Model of autism: increased ratio of excitation/inhibition in key neural systems
Rubenstein, J. L. R., & Merzenich, M. M. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00037.x · Cited by 2,768
Habituation: a model phenomenon for the study of neuronal substrates of behavior
Thompson, R. F., & Spencer, W. A. (1966) · Psychological Review · doi:10.1037/h0022681 · Cited by 2,608 · cited 6×
“This provides an explanation for the psychological phenomena of dishabituation and attentional override, two defining properties of habituation (Ramaswami, 2014; Rankin et al., 2009; Thompson and Spencer, 1966).”
BackgroundInfluential
Neocortical excitation/inhibition balance in information processing and social dysfunction
Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O’Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., et al. (2011) · Nature · doi:10.1038/nature10360 · Cited by 2,454
Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity
van Vreeswijk, C., & Sompolinsky, H. (1996) · Science · doi:10.1126/science.274.5293.1724 · Cited by 1,831
Rare Structural Variants Disrupt Multiple Genes in Neurodevelopmental Pathways in Schizophrenia
Walsh, T., McClellan, J. M., McCarthy, S. E., Addington, A. M., Pierce, S. B., Cooper, G. M., Nord, A. S., Kusenda, M., Malhotra, D., Bhandari, A., et al. (2008) · Science · doi:10.1126/science.1155174 · Cited by 1,800
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669
Habituation revisited: An updated and revised description of the behavioral characteristics of habituation
Rankin, C. H., Abrams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., Coppola, G., Geyer, M. A., Glanzman, D. L., Marsland, S., et al. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.09.012 · Cited by 1,665
Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex
Wehr, M., & Zador, A. M. (2003) · Nature · doi:10.1038/nature02116 · Cited by 1,413
Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons
Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., & Scanziani, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3446 · Cited by 1,353
EEG evidence for mirror neuron dysfunction in autism spectrum disorders
Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.01.014 · Cited by 1,146
Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function
Turrigiano, G. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005736 · Cited by 1,139
Cortical interneurons that specialize in disinhibitory control
Pi, H.-J., Hangya, B., Kvitsiani, D., Sanders, J. I., Huang, Z. J., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12676 · Cited by 1,136
Engrams and circuits crucial for systems consolidation of a memory
Kitamura, T., Ogawa, S. K., Roy, D. S., Okuyama, T., Morrissey, M. D., Smith, L. M., Redondo, R. L., & Tonegawa, S. (2017) · Science · doi:10.1126/science.aam6808 · Cited by 1,104
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Pouille, F., & Scanziani, M. (2001) · Science · doi:10.1126/science.1060342 · Cited by 1,097
Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits
Peñagarikano, O., Abrahams, B. S., Herman, E. I., Winden, K. D., Gdalyahu, A., Dong, H., Sonnenblick, L. I., Gruver, R., Almajano, J., Bragin, A., et al. (2011) · Cell · doi:10.1016/j.cell.2011.08.040 · Cited by 1,075
Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia
Lisman, J. E., Coyle, J. T., Green, R. W., Javitt, D. C., Benes, F. M., Heckers, S., & Grace, A. A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.02.005 · Cited by 1,010
Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders
Nelson, S. B., & Valakh, V. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.033 · Cited by 1,001
Engineering a memory with LTD and LTP
Nabavi, S., Fox, R., Proulx, C. D., Lin, J. Y., Tsien, R. Y., & Malinow, R. (2014) · Nature · doi:10.1038/nature13294 · Cited by 980
A Cortical Circuit for Gain Control by Behavioral State
Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., Huang, Z. J., & Stryker, M. P. (2014) · Cell · doi:10.1016/j.cell.2014.01.050 · Cited by 937
Engram cells retain memory under retrograde amnesia
Ryan, T. J., Roy, D. S., Pignatelli, M., Arons, A. L., & Tonegawa, S. (2015) · Science · doi:10.1126/science.aaa5542 · Cited by 789
Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks
Vogels, T. P., Sprekeler, H., Zenke, F., Clopath, C., & Wulfram Gerstner, B. (2011) · Science · doi:10.1126/science.1211095 · Cited by 763
Self-citation
Equalizing excitation-inhibition ratios across visual cortical neurons
Xue, M., Atallah, B. V., & Scanziani, M. (2014) · Nature · doi:10.1038/nature13321 · Cited by 722
Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities
Okun, M., & Lampl, I. (2008) · Nature Neuroscience · doi:10.1038/nn.2105 · Cited by 701
Memory retrieval by activating engram cells in mouse models of early Alzheimer’s disease
Roy, D. S., Arons, A. L., Mitchell, T. I., Pignatelli, M., Ryan, T. J., & Tonegawa, S. (2016) · Nature · doi:10.1038/nature17172 · Cited by 620
Schema-dependent gene activation and memory encoding in neocortex
Tse, D., Takeuchi, T., Kakeyama, M., Kajii, Y., Okuno, H., Tohyama, C., Bito, H., & Morris, R. G. M. (2011) · Science · doi:10.1126/science.1205274 · Cited by 618
Common circuit defect of excitatory-inhibitory balance in mouse models of autism
Gogolla, N., LeBlanc, J. J., Quast, K. B., Südhof, T. C., Fagiolini, M., & Hensch, T. K. (2009) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-009-9023-x · Cited by 610
Oxytocin-Mediated GABA Inhibition During Delivery Attenuates Autism Pathogenesis in Rodent Offspring
Tyzio, R., Nardou, R., Ferrari, D. C., Tsintsadze, T., Shahrokhi, A., Eftekhari, S., Khalilov, I., Tsintsadze, V., Brouchoud, C., Chazal, G., et al. (2014) · Science · doi:10.1126/science.1247190 · Cited by 601
A synaptic memory trace for cortical receptive field plasticity
Froemke, R. C., Merzenich, M. M., & Schreiner, C. E. (2007) · Nature · doi:10.1038/nature06289 · Cited by 600
Autism as a disorder of prediction
Sinha, P., Kjelgaard, M. M., Gandhi, T. K., Tsourides, K., Cardinaux, A. L., Pantazis, D., Diamond, S. P., & Held, R. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416797111 · Cited by 563
Impaired disengagement of attention in young children with autism
Landry, R., & Bryson, S. E. (2004) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2004.00304.x · Cited by 545 · cited 1×
“…of autism such as sticky attention, wherein familar stimuli remain engaging for unusually long periods of time while novel stimuli seem challenging, could arise from weak habituation and hypersensitivity to novel stimuli (Landry and Bryson, 2004; Sinha et al., 2014; Vogels and Abbott, 2007).”
Background
A neuronal model of predictive coding accounting for the mismatch negativity.
Wacongne, C., Changeux, J.-P., & Dehaene, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5003-11.2012 · Cited by 542
Common Mechanisms of Excitatory and Inhibitory Imbalance in Schizophrenia and Autism Spectrum Disorders
Gao, R., & Penzes, P. (2015) · Current Molecular Medicine · doi:10.2174/1566524015666150303003028 · Cited by 516 · cited 2×
“This is consistent with theoretical models in which EI imbalance in neural networks has been used to account for hallucinations and delusional experiences that may be observed both in autism and in schizophrenia (Gao and Penzes, 2015; Toal et al., 2009; Vogels and Abbott, 2007).”
BackgroundResult
Amygdala interneuron subtypes control fear learning through disinhibition
Wolff, S. B. E., Gründemann, J., Tovote, P., Krabbe, S., Jacobson, G. A., Müller, C. R., Herry, C., Ehrlich, I., Friedrich, R. W., Letzkus, J. J., et al. (2014) · Nature · doi:10.1038/nature13258 · Cited by 515
Prefrontal Regions Orchestrate Suppression of Emotional Memories via a Two-Phase Process
Depue, B. E., Curran, T., & Banich, M. T. (2007) · Science · doi:10.1126/science.1139560 · Cited by 467
Disinhibition, a Circuit Mechanism for Associative Learning and Memory
Letzkus, J. J., Wolff, S. B. E., & Lüthi, A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.024 · Cited by 430
Coincident Pre- and Postsynaptic Activity Modifies GABAergic Synapses by Postsynaptic Changes in Cl− Transporter Activity
Woodin, M. A., Ganguly, K., & Poo, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00507-5 · Cited by 427
Early Tagging of Cortical Networks Is Required for the Formation of Enduring Associative Memory
Lesburguères, E., Gobbo, O. L., Alaux‐Cantin, S., Hambücken, A., Trifilieff, P., & Bontempi, B. (2011) · Science · doi:10.1126/science.1196164 · Cited by 412
The intense world syndrome-an alternative hypothesis for autism
Markram, H. (2007) · Frontiers in Neuroscience · doi:10.3389/neuro.01.1.1.006.2007 · Cited by 394
Gating multiple signals through detailed balance of excitation and inhibition in spiking networks
Vogels, T. P., & Abbott, L. F. (2009) · Nature Neuroscience · doi:10.1038/nn.2276 · Cited by 375
Self-citation
Parallel processing by cortical inhibition enables context-dependent behavior
Kuchibhotla, K. V., Gill, J. V., Lindsay, G. W., Papadoyannis, E. S., Field, R. E., Sten, T. H., Miller, K. D., & Froemke, R. C. (2016) · Nature Neuroscience · doi:10.1038/nn.4436 · Cited by 366
Opposing Mechanisms Support the Voluntary Forgetting of Unwanted Memories
Benoit, R. G., & Anderson, M. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.025 · Cited by 363
Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe
Chou, Y.-H., Spletter, M. L., Yaksi, E., Leong, J. C. S., Wilson, R. I., & Luo, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2489 · Cited by 361
Spatio-Temporal Subthreshold Receptive Fields in the Vibrissa Representation of Rat Primary Somatosensory Cortex
Moore, C. I., & Nelson, S. B. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.6.2882 · Cited by 322
Opioids block long-term potentiation of inhibitory synapses
Nugent, F. S., Penick, E. C., & Kauer, J. A. (2007) · Nature · doi:10.1038/nature05726 · Cited by 297
Genes, circuits, and precision therapies for autism and related neurodevelopmental disorders
Sahin, M., & Sur, M. (2015) · Science · doi:10.1126/science.aab3897 · Cited by 295
Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Eschenko, O., Ramadan, W., Mölle, M., Born, J., & Sara, S. J. (2008) · Learning & Memory · doi:10.1101/lm.726008 · Cited by 277
Prefrontal–hippocampal pathways underlying inhibitory control over memory
Anderson, M. C., Bunce, J. G., & Barbas, H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.008 · Cited by 269
Flexible Sensory Representations in Auditory Cortex Driven by Behavioral Relevance
Kato, H., Gillet, S. N., & Isaacson, J. S. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.024 · Cited by 257
Reduced Neural Habituation in the Amygdala and Social Impairments in Autism Spectrum Disorders
Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., & Aylward, E. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.07101681 · Cited by 255
Strength through Diversity
Nelson, S. B., & Turrigiano, G. G. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.020 · Cited by 233
Enhancement of Inhibitory Neurotransmission by GABA A Receptors Having α 2,3 -Subunits Ameliorates Behavioral Deficits in a Mouse Model of Autism
Han, S., Tai, C., Jones, C. J., Scheuer, T., & Catterall, W. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.016 · Cited by 231
Repetition suppression: a means to index neural representations using BOLD?
Barron, H. C., Garvert, M. M., & Behrens, T. E. J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0355 · Cited by 229
Self-citation
Aversive Learning and Appetitive Motivation Toggle Feed-Forward Inhibition in the Drosophila Mushroom Body
Perisse, E., Owald, D., Barnstedt, O., Talbot, C. B., Huetteroth, W., & Waddell, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.034 · Cited by 227
Plasticity of local GABAergic interneurons drives olfactory habituation
Das, S., Sadanandappa, M. K., Dervan, A., Larkin, A., Lee, J. A., Sudhakaran, I. P., Priya, R., Heidari, R., Holohan, E. E., Pimentel, A., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106411108 · Cited by 219
Self-citation
Inhibitory and Excitatory Spike-Timing-Dependent Plasticity in the Auditory Cortex
D’amour, J. A., & Froemke, R. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.014 · Cited by 210
An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity
Chen, N., Sugihara, H., & Sur, M. (2015) · Nature Neuroscience · doi:10.1038/nn.4002 · Cited by 210
Perisomatic GABA Release and Thalamocortical Integration onto Neocortical Excitatory Cells Are Regulated by Neuromodulators
Kruglikov, I., & Rudy, B. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.024 · Cited by 209
Reduced habituation of auditory evoked potentials indicate cortical hyper-excitability in Fragile X Syndrome.
Ethridge, L. E., White, S. P., Mosconi, M. W., Wang, J., Byerly, M. J., & Sweeney, J. A. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.48 · Cited by 188
Network plasticity in adaptive filtering and behavioral habituation.
Ramaswami, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.035 · Cited by 183
Self-citation
Jointly reduced inhibition and excitation underlies circuit-wide changes in cortical processing in Rett syndrome
Banerjee, A., Rikhye, R. V., Breton‐Provencher, V., Tang, X., Li, C., Li, K., Runyan, C. A., Fu, Z., Jaenisch, R., & Sur, M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1615330113 · Cited by 182
Adaptive Top–Down Suppression of Hippocampal Activity and the Purging of Intrusive Memories from Consciousness
Benoit, R. G., Hulbert, J. C., Huddleston, E., & Anderson, M. C. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00696 · Cited by 174
Hippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory
Ramadan, W., Eschenko, O., & Sara, S. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006697 · Cited by 173
Autism and epilepsy: Historical perspective
Tuchman, R., Cuccaro, M., & Alessandri, M. (2010) · Brain and Development · doi:10.1016/j.braindev.2010.04.008 · Cited by 172
Visual recognition memory, manifested as long-term habituation, requires synaptic plasticity in V1
Cooke, S. F., Komorowski, R. W., Kaplan, E. S., Gavornik, J. P., & Bear, M. F. (2015) · Nature Neuroscience · doi:10.1038/nn.3920 · Cited by 152
Selectivity of Neuromodulatory Projections from the Basal Forebrain and Locus Ceruleus to Primary Sensory Cortices
Kim, J., Jung, A.-H., Jeong, D., Choi, I., Kim, K., Shin, S., Kim, S. J., & Lee, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4333-15.2016 · Cited by 148
Inhibitory synaptic plasticity: spike timing-dependence and putative network function
Vogels, T. P., Froemke, R. C., Doyon, N., Gilson, M., Haas, J. S., Liu, R., Maffei, A., Miller, P. C., Wierenga, C. J., Woodin, M. A., et al. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00119 · Cited by 141
Self-citation
Inhibition protects acquired song segments during vocal learning in zebra finches
Vallentin, D., Kosche, G., Lipkind, D., & Long, M. A. (2016) · Science · doi:10.1126/science.aad3023 · Cited by 140
Unmasking Latent Inhibitory Connections in Human Cortex to Reveal Dormant Cortical Memories
Barron, H. C., Vogels, T. P., Emir, U. E., Makin, T. R., O’Shea, J., Clare, S., Jbabdi, S., Dolan, R. J., & Behrens, T. E. J. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.031 · Cited by 133
Self-citation
Differential habituation to repeated sounds in infants at high risk for autism
Guiraud, J. A., Kushnerenko, E., Tomalski, P., Davies, K., Ribeiro, H., & Johnson, M. H. (2011) · NeuroReport · doi:10.1097/wnr.0b013e32834c0bec · Cited by 130
The innervation of parvalbumin-containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat
Dávid, C., Schleicher, A., Zuschratter, W., & Staiger, J. F. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05496.x · Cited by 120
Is predictive coding theory articulated enough to be testable?
Kogo, N., & Trengove, C. (2015) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2015.00111 · Cited by 98 · cited 2×
“Although we focus here on inhibitory engrams created by local EI balancing mechanisms, the framework we propose also naturally accommodates inhibitory representations constructed through potential alternative mechanisms (Clark, 2013; Cooke et al., 2015; Kogo and Trengove, 2015; Ramaswami, 2014; Rao and Ballard, 1999;…”
Background
LTP of GABAergic synapses in the ventral tegmental area and beyond
Nugent, F. S., & Kauer, J. A. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.148098 · Cited by 91
Balancing Feed-Forward Excitation and Inhibition via Hebbian Inhibitory Synaptic Plasticity
Luz, Y., & Shamir, M. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002334 · Cited by 89
Psychosis and autism: magnetic resonance imaging study of brain anatomy
Toal, F., Bloemen, O., Deeley, Q., Tunstall, N., Daly, E., Page, L., Brammer, M. J., Murphy, K. C., & Murphy, D. (2009) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.107.049007 · Cited by 83
Metaplasticity at identified inhibitory synapses in Aplysia
Fischer, T. M., Blazis, D. E. J., Priver, N. A., & Carew, T. J. (1997) · Nature · doi:10.1038/39892 · Cited by 71
Activity-dependent potentiation of recurrent inhibition: a mechanism for dynamic gain control in the siphon withdrawal reflex of Aplysia
Fischer, T., & Carew, T. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-01302.1993 · Cited by 67
Persistence of amygdala gamma oscillations during extinction learning predicts spontaneous fear recovery
Courtin, J., Karalis, N., Gonzalez-Campo, C., Wurtz, H., & Herry, C. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.015 · Cited by 65
Plasticity of Recurrent Inhibition in theDrosophilaAntennal Lobe
Sudhakaran, I. P., Holohan, E. E., Osman, S., Rodrigues, V., VijayRaghavan, K., & Ramaswami, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1099-12.2012 · Cited by 62
Self-citation
Central synaptic mechanisms underlie short-term olfactory habituation in Drosophila larvaePreprint
Larkin, A., Karak, S., Priya, R., Das, A., Ayyub, C., Ito, K., Rodrigues, V., & Ramaswami, M. (2010) · Learning & Memory · doi:10.1101/lm.1839010 · Cited by 56
Self-citation
Mechanisms of Plasticity in the Developing and Adult Visual Cortex
Sur, M., Nagakura, I., Chen, N., & 杉原, 弘. (2013) · Progress in brain research · doi:10.1016/b978-0-444-63327-9.00002-3 · Cited by 44
Placing memories in context: Hippocampal representations promote retrieval of appropriate memories
Bulkin, D. A., Law, L. M., & Smith, D. M. (2016) · Hippocampus · doi:10.1002/hipo.22579 · Cited by 32
Early Memories of Individuals on the Autism Spectrum Assessed Using Online Self-Reports
Zamoscik, V., Mier, D. U., Schmidt, S. N. L., & Kirsch, P. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00079 · Cited by 24
Differential role of inhibition in habituation of two independent afferent pathways to a common motor outputPreprint
Bristol, A. S., & Carew, T. J. (2005) · Learning & Memory · doi:10.1101/lm.83405 · Cited by 21
Gating Deficits in Model Networks: A Path to Schizophrenia?
Vogels, T. P., & Abbott, L. F. (2007) · Pharmacopsychiatry · doi:10.1055/s-2007-992130 · Cited by 20
Self-citation
Olfactory habituation: Fresh insights from flies
Glanzman, D. L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111230108 · Cited by 19

Research works printed but not linked: 1

R Semon, Engraphic action of stimuli on the individual. The Mneme, ed TbL Simon (George Allen and Unwin, London, 1921).

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Authors: Barron, H. C., Vogels, T. P., Behrens, T. E., & Ramaswami, M.
Affiliations: University of Oxford (GB)
Wellcome Centre for Human Neuroimaging (GB)
Tata Institute of Fundamental Research (IN)
ORCID: Barron, Helen C.
Vogels, Tim P.
Behrens, Timothy E.
Ramaswami, Mani
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2017-06-13
Volume: 114
Issue: 26
Pages: 6666-6674
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1701812114
PMC: PMC5495250
OpenAlex: W2626706140
Cited by: 147
References: 91
Citations by year: 2026: 17 · 2025: 17 · 2024: 23 · 2023: 12 · 2022: 22 · 2021: 17 · 2020: 17 · 2019: 10 · 2018: 11 · 2017: 1
FWCI: 1.19
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.pnas.org/site/misc/userlicense.xhtml (vor, 183 d)
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: John Fell Fund, University of Oxford (John Fell OUP Research Fund) (153/046)
Wellcome Trust (WT100000, WT104765MA)
James S. McDonnell Foundation (JSMF) (JSMF220020372)
Science Foundation Ireland (SFI) (15/IA/3123)
Department of Atomic Energy, Government of India (DAE) (Core Funds to TIFR/NCBS)
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 › Neural dynamics and brain function
Keywords: memory engrams, cell assemblies, habituation, latent memory, disinhibition, perception, excitation-inhibition balance, autism spectrum disorder, schizophrenia, post-traumatic stress disorder, transdiagnostic traits
MeSH terms: Animals, Autistic Disorder, Cognition, Humans, Memory, Models, Neurological, Nerve Net, Perception, Schizophrenia, Stress Disorders, Post-Traumatic

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Inhibitory engrams in perception and memory

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