Coordinated neuronal ensembles in primary auditory cortical columns
Abstract
Synchronous activity of groups of neurons is increasingly thought to be important in cortical information processing and transmission. However, most studies of processing in the primary auditory cortex (AI) have viewed neurons as independent filters; little is known about how coordinated AI neuronal activity is expressed throughout cortical columns and how it might enhance the processing of auditory information. To address this, we recorded from populations of neurons in AI cortical columns of anesthetized rats and, using dimensionality reduction techniques, identified multiple coordinated neuronal ensembles (cNEs), i.e. groups of neurons with reliable synchronous activity. We show that cNEs reflect local network configurations with enhanced information encoding properties that cannot be accounted for by stimulus-driven synchronization alone. Furthermore, similar cNEs were identified in both spontaneous and evoked activity, indicating that columnar cNEs are stable functional constructs that may represent principal units of information processing in AI.
Data availability
Single-unit extracellular electrophysiological data have been deposited in CRCNS.org under DOI citation http://dx.doi.org/10.6080/K09021X1
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High-density extracellular recordings from the primary auditory cortex in anesthetized rats listening to dynamic broadband stimuli.Publicly available at the Collaborative Research in Computational Neuroscience data sharing website (http://crcns.org/).
Article and author information
Author details
Funding
National Institute on Deafness and Other Communication Disorders (DC02260)
- Craig A Atencio
- Christoph E Schreiner
Coleman Memorial Fund
- Craig A Atencio
- Christoph E Schreiner
Hearing Research Incorporate, San Francisco
- Craig A Atencio
- Christoph E Schreiner
Agency for Science, Technology and Research, Singapore (National Science Scholarship)
- Jermyn Z See
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Catherine Emily Carr, University of Maryland, United States
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#100-17) of the University of California, San Francisco. The protocol was approved by the IACUC of the University of California, San Francisco (Protocol Number: AN165706-02). All surgery was performed under ketamine/xylazine anesthesia, and every effort was made to minimize suffering.
Version history
- Received: February 1, 2018
- Accepted: June 3, 2018
- Accepted Manuscript published: June 5, 2018 (version 1)
- Version of Record published: June 25, 2018 (version 2)
Copyright
© 2018, See et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
Synaptic inputs to cortical neurons are highly structured in adult sensory systems, such that neighboring synapses along dendrites are activated by similar stimuli. This organization of synaptic inputs, called synaptic clustering, is required for high-fidelity signal processing, and clustered synapses can already be observed before eye opening. However, how clustered inputs emerge during development is unknown. Here, we employed concurrent in vivo whole-cell patch-clamp and dendritic calcium imaging to map spontaneous synaptic inputs to dendrites of layer 2/3 neurons in the mouse primary visual cortex during the second postnatal week until eye opening. We found that the number of functional synapses and the frequency of transmission events increase several fold during this developmental period. At the beginning of the second postnatal week, synapses assemble specifically in confined dendritic segments, whereas other segments are devoid of synapses. By the end of the second postnatal week, just before eye opening, dendrites are almost entirely covered by domains of co-active synapses. Finally, co-activity with their neighbor synapses correlates with synaptic stabilization and potentiation. Thus, clustered synapses form in distinct functional domains presumably to equip dendrites with computational modules for high-capacity sensory processing when the eyes open.
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- Neuroscience
Accurate tracking of the same neurons across multiple days is crucial for studying changes in neuronal activity during learning and adaptation. Advances in high-density extracellular electrophysiology recording probes, such as Neuropixels, provide a promising avenue to accomplish this goal. Identifying the same neurons in multiple recordings is, however, complicated by non-rigid movement of the tissue relative to the recording sites (drift) and loss of signal from some neurons. Here, we propose a neuron tracking method that can identify the same cells independent of firing statistics, that are used by most existing methods. Our method is based on between-day non-rigid alignment of spike-sorted clusters. We verified the same cell identity in mice using measured visual receptive fields. This method succeeds on datasets separated from 1 to 47 days, with an 84% average recovery rate.