Coding of envelopes by correlated but not single-neuron activity requires neural variability

Michael G. Metzen, Mohsen Jamali, Jérome Carriot, Oscar Ávila-Åkerberg, Kathleen Cullen, Maurice J. Chacron

Research output: Contribution to journalArticle

Abstract

Understanding how the brain processes sensory information is often complicated by the fact that neurons exhibit trial-to-trial variability in their responses to stimuli. Indeed, the role of variability in sensory coding is still highly debated. Here, we examined how variability influences neural responses to naturalistic stimuli consisting of a fast time-varying waveform (i.e., carrier or first order) whose amplitude (i.e., envelope or second order) varies more slowly. Recordings were made from fish electrosensory and monkey vestibular sensory neurons. In both systems, we show that correlated but not single-neuron activity can provide detailed information about second-order stimulus features. Using a simple mathematical model, we made the strong prediction that such correlation-based coding of envelopes requires neural variability. Strikingly, the performance of correlated activity at predicting the envelope was similarly optimally tuned to a nonzero level of variability in both systems, thereby confirming this prediction. Finally, we show that second-order sensory information can only be decoded if one takes into account joint statistics when combining neural activities. Our results thus show that correlated but not single-neural activity can transmit information about the envelope, that such transmission requires neural variability, and that this information can be decoded. We suggest that envelope coding by correlated activity is a general feature of sensory processing that will be found across species and systems.

Original languageEnglish (US)
Pages (from-to)4791-4796
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number15
DOIs
StatePublished - Apr 14 2015
Externally publishedYes

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Neurons
Sensory Receptor Cells
Synaptic Transmission
Haplorhini
Fishes
Theoretical Models
Joints
Brain

Keywords

  • Correlation
  • Electrosensory
  • Envelope
  • Neural coding
  • Vestibular

ASJC Scopus subject areas

  • General
  • Medicine(all)

Cite this

Coding of envelopes by correlated but not single-neuron activity requires neural variability. / Metzen, Michael G.; Jamali, Mohsen; Carriot, Jérome; Ávila-Åkerberg, Oscar; Cullen, Kathleen; Chacron, Maurice J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 15, 14.04.2015, p. 4791-4796.

Research output: Contribution to journalArticle

Metzen, Michael G. ; Jamali, Mohsen ; Carriot, Jérome ; Ávila-Åkerberg, Oscar ; Cullen, Kathleen ; Chacron, Maurice J. / Coding of envelopes by correlated but not single-neuron activity requires neural variability. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 15. pp. 4791-4796.
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