A synaptic memory trace for cortical receptive field plasticity
Abstract
Receptive fields of sensory cortical neurons are plastic, changing in response to alterations of neural activity or sensory experience. In this way, cortical representations of the sensory environment can incorporate new information about the world, depending on the relevance or value of particular stimuli. Neuromodulation is required for cortical plasticity, but it is uncertain how subcortical neuromodulatory systems, such as the cholinergic nucleus basalis, interact with and refine cortical circuits. Here we determine the dynamics of synaptic receptive field plasticity in the adult primary auditory cortex (also known as AI) using in vivo whole-cell recording. Pairing sensory stimulation with nucleus basalis activation shifted the preferred stimuli of cortical neurons by inducing a rapid reduction of synaptic inhibition within seconds, which was followed by a large increase in excitation, both specific to the paired stimulus. Although nucleus basalis was stimulated only for a few minutes, reorganization of synaptic tuning curves progressed for hours thereafter: inhibition slowly increased in an activity-dependent manner to rebalance the persistent enhancement of excitation, leading to a retuned receptive field with new preference for the paired stimulus. This restricted period of disinhibition may be a fundamental mechanism for receptive field plasticity, and could serve as a memory trace for stimuli or episodes that have acquired new behavioural significance.
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In the auditory cortex, pairing sensory stimulation with stimulation of the basal forebrain results in a long-term reorganization of cortical receptive field structure, including a persistent shift in the receptive field towards the paired stimulus.
“In the auditory cortex, pairing sensory stimulation with stimulation of the basal forebrain results in a long-term reorganization of cortical receptive field structure, including a persistent shift in the receptive field towards the paired stimulus (Froemke et al., 2007).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Froemke et al., 2007
ACh modulates cortical circuits over longer time scales by influencing the plasticity of cortical circuits.
“ACh also modulates cortical circuits over longer time scales by influencing the plasticity of cortical circuits.”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Froemke et al., 2007
Collectively, these changes could increase inhibition in association cortex and mediate transient enhancement and developmental reduction of plasticity in a manner similar to sensory cortex.
“Collectively, these changes could increase inhibition in association cortex and mediate transient enhancement and developmental reduction of plasticity (Dorrn et al., 2010; Froemke et al., 2007; Gandhi et al., 2008; Hensch, 2005; Southwell et al., 2010) in a manner similar to sensory cortex (Levelt and Hubener, 2012) .”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Froemke et al., 2007
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Cites
Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968 · see citing works
CORTICAL PLASTICITY: From Synapses to Maps
Buonomano, D. V., & Merzenich, M. M. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.149 · Cited by 2,083 · see citing works
Self-citationUncertainty, Neuromodulation, and Attention
Yu, A. J., & Dayan, P. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.026 · Cited by 1,774 · see citing works
Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex
Wehr, M., & Zador, A. M. (2003) · Nature · doi:10.1038/nature02116 · Cited by 1,363 · 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
Cortical Map Reorganization Enabled by Nucleus Basalis Activity
Kilgard, M. P., & Merzenich, M. M. (1998) · Science · doi:10.1126/science.279.5357.1714 · Cited by 1,197 · see citing works
Self-citationModulation of visual cortical plasticity by acetylcholine and noradrenaline
Bear, M. F., & Singer, W. (1986) · Nature · doi:10.1038/320172a0 · Cited by 858 · see citing works
Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex
Fritz, J. B., Shamma, S., Elhilali, M., & Klein, D. (2003) · Nature Neuroscience · doi:10.1038/nn1141 · Cited by 825 · see citing works
Sarter, M., Hasselmo, M. E., Bruno, J. P., & Givens, B. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.08.006 · Cited by 667 · see citing works
Specific long-term memory traces in primary auditory cortex
Weinberger, N. M. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1366 · Cited by 600 · see citing works
Metherate, R., Cox, C. L., & Ashe, J. H. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04701.1992 · Cited by 575 · see citing works
Environmental Noise Retards Auditory Cortical Development
Chang, E. F., & Merzenich, M. M. (2003) · Science · doi:10.1126/science.1082163 · Cited by 573 · see citing works
Self-citationCholinergic Basal Forebrain Neurons Burst with Theta during Waking and Paradoxical Sleep
Lee, M., Hassani, O. K., Alonso, Á., & Jones, B. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0178-05.2005 · Cited by 439 · see citing works
Cholinergic Switching Within Neocortical Inhibitory Networks
Xiang, Z., Huguenard, J. R., & Prince, D. A. (1998) · Science · doi:10.1126/science.281.5379.985 · Cited by 438 · see citing works
Gilbert, C. D. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.2.467 · Cited by 383 · see citing works
Multiparametric corticofugal modulation and plasticity in the auditory system
Suga, N., & Ma, X. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1222 · Cited by 380 · see citing works
Critical Period Window for Spectral Tuning Defined in the Primary Auditory Cortex (A1) in the Rat
de Villers‐Sidani, E., Chang, E. F., Bao, S., & Merzenich, M. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3227-06.2007 · Cited by 378 · see citing works
Self-citationBinary Spiking in Auditory Cortex
DeWeese, M. R., Wehr, M., & Zador, A. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07940.2003 · Cited by 355 · see citing works
Thompson, R. F. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070239 · Cited by 314 · see citing works
Tone-Evoked Excitatory and Inhibitory Synaptic Conductances of Primary Auditory Cortex Neurons
Tan, A. Y. Y., Zhang, L. I., Merzenich, M. M., & Schreiner, C. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01020.2003 · Cited by 272 · see citing works
Self-citationThe 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
Contribution of Individual Spikes in Burst-Induced Long-Term Synaptic Modification
Froemke, R. C., Tsay, I. A., Raad, M., Long, J. D., & Dan, Y. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00910.2005 · Cited by 213 · see citing works
Self-citationExperience-Dependent Plasticity in Adult Visual Cortex
Karmarkar, U. R., & Dan, Y. (2006) · Neuron · doi:10.1016/j.neuron.2006.11.001 · Cited by 208 · see citing works
Gritti, I., Manns, I. D., Mainville, L., & Jones, B. E. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10505 · Cited by 178 · see citing works
Meliza, C. D., & Dan, Y. (2006) · Neuron · doi:10.1016/j.neuron.2005.12.009 · Cited by 177 · see citing works
Development of spectral and temporal response selectivity in the auditory cortex
Chang, E. F., Bao, S., Imaizumi, K., Schreiner, C. E., & Merzenich, M. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508239102 · Cited by 171 · see citing works
Self-citationA reappraisal of the functions of the nucleus basalis of Meynert
Richardson, R. T., & DeLong, M. R. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90107-5 · Cited by 154 · see citing works
Schreiner, C. E., & Sutter, M. L. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.5.1487 · Cited by 148 · see citing works
Self-citationSpectral integration in auditory cortex: Mechanisms and modulation
Metherate, R., Kaur, S., Kawai, H. D., Lazar, R., Liang, K., & Rose, H. J. (2005) · Hearing Research · doi:10.1016/j.heares.2005.01.014 · Cited by 99 · see citing works
Activity‐dependent regulation of ‘on’ and ‘off’ responses in cat visual cortical receptive fields
Debanne, D., Shulz, D. E., & Frégnac, Y. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.00523.x · Cited by 49 · see citing works
Woody, C. D., & Gruen, E. (1987) · Brain Research · doi:10.1016/0006-8993(87)91210-8 · Cited by 37 · see citing works
Zhang, Y. F., Hamilton, S. E., Nathanson, N. M., & Yan, J. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj067 · Cited by 35 · see citing works
Toward the mechanisms of auditory attention
Hromádka, T., & Zador, A. M. (2007) · Hearing Research · doi:10.1016/j.heares.2007.01.002 · Cited by 28 · see citing works
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Neuronal circuits for fear and anxiety
Tovote, P., Fadok, J. P., & Lüthi, A. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3945 · Cited by 1,786 · see citing works
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
A disinhibitory microcircuit for associative fear learning in the auditory cortex
Letzkus, J. J., Wolff, S. B. E., Meyer, E. M. M., Tovote, P., Courtin, J., Herry, C., & Lüthi, A. (2011) · Nature · doi:10.1038/nature10674 · Cited by 840 · see citing works
Oxytocin enables maternal behaviour by balancing cortical inhibition
Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C. (2015) · Nature · doi:10.1038/nature14402 · Cited by 744 · see citing works
Self-citationSynaptic mechanisms for plasticity in neocortex
Feldman, D. E. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135516 · Cited by 704 · see citing works
A synaptic and circuit basis for corollary discharge in the auditory cortex
Schneider, D. M., Nelson, A., & Mooney, R. (2014) · Nature · doi:10.1038/nature13724 · Cited by 580 · see citing works
Removing brakes on adult brain plasticity: From molecular to behavioral interventions
Bavelier, D., Levi, D. M., Li, R. W., Dan, Y., & Hensch, T. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4812-10.2010 · Cited by 589 · see citing works
Efficient codes and balanced networks
Denève, S., & Machens, C. K. (2016) · Nature Neuroscience · doi:10.1038/nn.4243 · Cited by 471 · see citing works
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Froemke, R. C. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034002 · Cited by 458 · see citing works
Self-citationExperimental evidence for sparse firing in the neocortex
Barth, A. L., & Poulet, J. F. A. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.03.008 · Cited by 364 · see citing works
A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex
Kuhlman, S. J., Olivas, N. D., Tring, E., Ikrar, T., Xu, X., & Trachtenberg, J. T. (2013) · Nature · doi:10.1038/nature12485 · Cited by 412 · see citing works
Long-term potentiation and long-term depression: a clinical perspective
Bliss, T. V. P., & Cooke, S. F. (2011) · Clinics · doi:10.1590/s1807-59322011001300002 · Cited by 333 · see citing works
Developmental sensory experience balances cortical excitation and inhibition
Dorrn, A. L., Yuan, K., Barker, A. J., Schreiner, C. E., & Froemke, R. C. (2010) · Nature · doi:10.1038/nature09119 · Cited by 296 · see citing works
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Anaclet, C., Pedersen, N. P., Ferrari, L. L., Venner, A., Bass, C. E., Arrigoni, E., & Fuller, P. M. (2015) · Nature Communications · doi:10.1038/ncomms9744 · Cited by 273 · see citing works
Cortical Plasticity Induced by Inhibitory Neuron Transplantation
Southwell, D. G., Froemke, R. C., Alvarez-Buylla, A., Stryker, M. P., & Gandhi, S. P. (2010) · Science · doi:10.1126/science.1183962 · Cited by 271 · see citing works
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Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
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Mongillo, G., Rumpel, S., & Loewenstein, Y. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0226-x · Cited by 148 · see citing works
Campanac, E., Gasselin, C., Baude, A., Rama, S., Ankri, N., & Debanne, D. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.020 · Cited by 150 · see citing works
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Barron, H. C., Vogels, T. P., Behrens, T. E., & Ramaswami, M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701812114 · Cited by 147 · see citing works
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Moczulska, K. E., Tinter-Thiede, J., Peter, M., Ushakova, L., Wernle, T., Bathellier, B., & Rumpel, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312508110 · Cited by 127 · see citing works
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Dulcis, D., & Spitzer, N. C. (2008) · Nature · doi:10.1038/nature07569 · Cited by 115 · see citing works
Wang, L., Conner, J. M., Rickert, J., & Tuszynski, M. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014335108 · Cited by 108 · see citing works
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Carcea, I., & Froemke, R. C. (2013) · Progress in Brain Research · doi:10.1016/b978-0-444-63327-9.00003-5 · Cited by 110 · see citing works
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- Authors
- Froemke, R. C., Merzenich, M. M., & Schreiner, C. E.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Froemke, Robert C.
- Venue
- Nature
- Published
- 2007-11-15
- Volume
- 450
- Issue
- 7168
- Pages
- 425-429
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2151934707
- Cited by
- 600
- References
- 33
- Citations by year
- 2026: 10 · 2025: 25 · 2024: 38 · 2023: 28 · 2022: 30 · 2021: 34 · 2020: 45 · 2019: 36 · 2018: 32 · 2017: 44 · 2016: 25 · 2015: 47 · 2014: 26 · 2013: 52 · 2012: 22
- FWCI
- 9.16
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (R01DC002260)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- receptive field plasticity, primary auditory cortex, nucleus basalis of Meynert, cholinergic modulation, synaptic inhibition, disinhibition, synaptic excitation, memory traces, sensory learning, activity-dependent plasticity
- MeSH terms
- Animals, Auditory Cortex, Female, Memory, Neuronal Plasticity, Neurons, Afferent, Synapses, Time Factors, Rats, Sprague-Dawley, Excitatory Postsynaptic Potentials, Rats
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