Developmental sensory experience balances cortical excitation and inhibition
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Early in life, neural circuits are highly susceptible to outside influences. The organization of the primary auditory cortex (A1) in particular is governed by acoustic experience during the critical period, an epoch near the beginning of postnatal development throughout which cortical synapses and networks are especially plastic. This neonatal sensitivity to the pattern of sensory inputs is believed to be essential for constructing stable and adequately adapted representations of the auditory world and for the acquisition of language skills by children. One important principle of synaptic organization in mature brains is the balance between excitation and inhibition, which controls receptive field structure and spatiotemporal flow of neural activity, but it is unknown how and when this excitatory-inhibitory balance is initially established and calibrated. Here we use whole-cell recording to determine the processes underlying the development of synaptic receptive fields in rat A1. We find that, immediately after the onset of hearing, sensory-evoked excitatory and inhibitory responses are equally strong, although inhibition is less stimulus-selective and mismatched with excitation. However, during the third week of postnatal development, excitation and inhibition become highly correlated. Patterned sensory stimulation drives coordinated synaptic changes across receptive fields, rapidly improves excitatory-inhibitory coupling and prevents further exposure-induced modifications. Thus, the pace of cortical synaptic receptive field development is set by progressive, experience-dependent refinement of intracortical inhibition.
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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 Dorrn et al., 2010
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- Authors
- Dorrn, A. L., Yuan, K., Barker, A. J., Schreiner, C. E., & Froemke, R. C.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Froemke, Robert C.
- Venue
- Nature
- Published
- 2010-06
- Volume
- 465
- Issue
- 7300
- Pages
- 932-936
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2888507
- OpenAlex
- W2001716460
- Cited by
- 296
- References
- 30
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 14 · 2023: 14 · 2022: 25 · 2021: 19 · 2020: 20 · 2019: 13 · 2018: 26 · 2017: 17 · 2016: 17 · 2015: 17 · 2014: 13 · 2013: 31 · 2012: 16
- FWCI
- 14.70
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (K99DC009635, R01DC002260)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- auditory cortex, excitation-inhibition balance, receptive field development, postnatal development, critical period, experience-dependent plasticity, inhibitory interneurons, synaptic inhibition, hearing onset, primary auditory cortex, rat auditory system, synaptic plasticity, sensory evoked potentials, language acquisition, neural circuit maturation, whole-cell recording, patch clamp
- MeSH terms
- Acoustic Stimulation, Animals, Auditory Cortex, Neural Inhibition, Rats, Sprague-Dawley, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Rats, Electrical Synapses
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