Single neurons may encode simultaneous stimuli by switching between activity patterns

Valeria C Caruso,Jeff T Mohl,Akinori F Ebihara,Shawn M Willett,Jennifer M Groh,Surya T Tokdar,Winrich A Freiwald,Rolando Estrada,Jungah Lee,Christopher Glynn,Azeem Zaman

doi:10.1038/s41467-018-05121-8

Abstract

How the brain preserves information about multiple simultaneous items is poorly understood. We report that single neurons can represent multiple stimuli by interleaving signals across time. We record single units in an auditory region, the inferior colliculus, while monkeys localize 1 or 2 simultaneous sounds. During dual-sound trials, we find that some neurons fluctuate between firing rates observed for each single sound, either on a whole-trial or on a sub-trial timescale. These fluctuations are correlated in pairs of neurons, can be predicted by the state of local field potentials prior to sound onset, and, in one monkey, can predict which sound will be reported first. We find corroborating evidence of fluctuating activity patterns in a separate dataset involving responses of inferotemporal cortex neurons to multiple visual stimuli. Alternation between activity patterns corresponding to each of multiple items may therefore be a general strategy to enhance the brain processing capacity, potentially linking such disparate phenomena as variable neural firing, neural oscillations, and limits in attentional/memory capacity.

Highlights

How the brain preserves information about multiple simultaneous items is poorly understood
Our results show that the activity patterns of inferior colliculus (IC) neurons fluctuate, and that these fluctuations may be consistent with encoding of multiple items in the same processing channels
The fluctuations are positively correlated across pairs of neurons, are reflective of the state of local field potentials at the time of sound onset, and are predictive of the behavioral response to follow

Summary

Introduction

How the brain preserves information about multiple simultaneous items is poorly understood. We investigated whether the brain solves this problem at the neuronal level via activity patterns that fluctuate between those evoked by each stimulus alone (Fig. 1a) If present, such fluctuations could allow each individual stimulus to be represented across time in a common neuronal ensemble. We found that a subpopulation of IC neurons exhibited fluctuating activity consistent with switching between individual sound responses at different time scales. We replicated the key observations regarding fluctuating activity in a separate data set involving inferotemporal cortex: neurons confronted with multiple object stimuli exhibited activity fluctuations consistent with switching between individual object responses. These observations support fluctuating activity as a viable and likely a general strategy for encoding simultaneously presented stimuli. We consider several broad implications of activity fluctuations for interpreting variability and other aspects of neural encoding

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