Abstract

The mechanisms by which the mammalian brain copes with information from natural vocalization streams remain poorly understood. This article shows that in highly vocal animals, such as the bat species Carollia perspicillata, the spike activity of auditory cortex neurons does not track the temporal information flow enclosed in fast time-varying vocalization streams emitted by conspecifics. For example, leading syllables of so-called distress sequences (produced by bats subjected to duress) suppress cortical spiking to lagging syllables. Local fields potentials (LFPs) recorded simultaneously to cortical spiking evoked by distress sequences carry multiplexed information, with response suppression occurring in low frequency LFPs (i.e. 2–15 Hz) and steady-state LFPs occurring at frequencies that match the rate of energy fluctuations in the incoming sound streams (i.e. >50 Hz). Such steady-state LFPs could reflect underlying synaptic activity that does not necessarily lead to cortical spiking in response to natural fast time-varying vocal sequences.

Highlights

  • The mechanisms by which the mammalian brain copes with information from natural vocalization streams remain poorly understood

  • Spike signals refer to action potentials generated by cortical neurons, while local field potentials (LFPs) result from the summation of synaptic activity in the cortex, activity in extra-cortical areas and the slow components of spikes produced by neurons near the recording electrodes[38,39,40]

  • These two sequences were chosen because they represent typical examples of a short distress sequence (Fig. 1a) and a long sequence containing multisyllabic bouts (Fig. 1b, see methods and[4] for a description of distress sequences produced by C. perspicillata)

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Summary

Introduction

The mechanisms by which the mammalian brain copes with information from natural vocalization streams remain poorly understood. Local fields potentials (LFPs) recorded simultaneously to cortical spiking evoked by distress sequences carry multiplexed information, with response suppression occurring in low frequency LFPs (i.e. 2–15 Hz) and steady-state LFPs occurring at frequencies that match the rate of energy fluctuations in the incoming sound streams In the AC, representing the information carried by single syllables embedded within a vocal sequence can be affected by phenomena such as forward suppression and adaptation These physiological phenomena cause a reduction of spike activity over time[32,33,34,35,36,37] and they could potentially affect the cortical representation of distress information. Our goal was to assess whether forward suppression decreases cortical spiking in response to lagging portions of the distress sequences (as it could be predicted from the currently available literature on forward suppression34,35,41,42), and whether this reduction in spike activity could prevent LFPs from being “entrained” by the www.nature.com/scientificreports/

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