Coordinated neuronal ensembles in primary auditory cortical columns
- University of California, San Francisco, United States
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
Christoph E Schreiner
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.
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.
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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Coordinated neuronal ensembles in primary auditory cortical columns
eLife 7:e35587.
https://doi.org/10.7554/eLife.35587
Further reading
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When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.
