Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development
Open accessAbstract
Functional receptive fields of neurons in sensory cortices undergo progressive refinement during development. Such refinement may be attributed to the pruning of non-optimal excitatory inputs, reshaping of the excitatory tuning profile through modifying the strengths of individual inputs, or strengthening of cortical inhibition. These models have not been directly tested because of the technical difficulties in assaying the spatiotemporal patterns of functional synaptic inputs during development. Here we apply in vivo whole-cell voltage-clamp recordings to the recipient layer 4 neurons in the rat primary auditory cortex (A1) to determine the developmental changes in the frequency-intensity tonal receptive fields (TRFs) of their excitatory and inhibitory inputs. Surprisingly, we observe co-tuned excitation and inhibition immediately after the onset of hearing, suggesting that a tripartite thalamocortical circuit with relatively strong feedforward inhibition is formed independently of auditory experience. The frequency ranges of tone-driven excitatory and inhibitory inputs first expand within a few days of the onset of hearing and then persist into adulthood. The latter phase is accompanied by a sharpening of the excitatory but not inhibitory frequency tuning profile, which results in relatively broader inhibitory tuning in adult A1 neurons. Thus the development of cortical synaptic TRFs after the onset of hearing is marked by a slight breakdown of previously formed excitation-inhibition balance. Our results suggest that functional refinement of cortical TRFs does not require a selective pruning of inputs, but may depend more on a fine adjustment of excitatory input strengths.
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Similar fine-tuning of excitation and inhibition is crucial for correct auditory cortical development.
“local GABAergic circuits modulate visual cortical plasticity in early postnatal life 9 , and similar fine-tuning of excitation and inhibition is also crucial for correct auditory cortical development 12 .”
From Progress toward treatments for synaptic defects in autism (2013) · cites this paper as [12]
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Self-citation
- Authors
- Sun, Y. J., Wu, G. K., Liu, B.-H., Li, P., Zhou, M., Xiao, Z., Tao, H. W., & Zhang, L. I.
- Affiliations
- University of Southern California (US)
- Southern Medical University (CN)
- Corresponding author
- Tao, Huizhong W.
- Zhang, Li I.
- Venue
- Nature
- Published
- 2010-06
- Volume
- 465
- Issue
- 7300
- Pages
- 927-931
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2909826
- OpenAlex
- W1967721763
- Cited by
- 180
- References
- 31
- Citations by year
- 2026: 3 · 2025: 12 · 2024: 4 · 2023: 4 · 2022: 10 · 2021: 9 · 2020: 9 · 2019: 8 · 2018: 15 · 2017: 12 · 2016: 8 · 2015: 15 · 2014: 13 · 2013: 25 · 2012: 10
- FWCI
- 10.30
- 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)
- Funders
- National Eye Institute (EY018718, R21EY018718, EY019049, R01EY019049)
- National Institute on Deafness and Other Communication Disorders (R03DC006814, R21DC008588, R01DC008983)
- National Center for Research Resources (UL1RR025755)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- primary auditory cortex, auditory cortex development, excitation-inhibition balance, feedforward inhibition, thalamocortical circuits, circuit plasticity, hearing onset, experience-dependent plasticity, neonatal rats, whole-cell voltage clamp
- MeSH terms
- Acoustic Stimulation, Animals, Auditory Cortex, Auditory Pathways, Hearing, Neural Inhibition, Sensory Receptor Cells, Time Factors, Rats, Sprague-Dawley, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Rats, Electrical Synapses
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