Abstract

Implicit expectations induced by predictable stimuli sequences affect neuronal response to upcoming stimuli at both single cell and neural population levels. Temporally regular sensory streams also phase entrain ongoing low frequency brain oscillations but how and why this happens is unknown. Here we investigate how random recurrent neural networks without plasticity respond to stimuli streams containing oddballs. We found the neuronal correlates of sensory stream adaptation emerge if networks generate chaotic oscillations which can be phase entrained by stimulus streams. The resultant activity patterns are close to critical and support history dependent response on long timescales. Because critical network entrainment is a slow process stimulus response adapts gradually over multiple repetitions. Repeated stimuli generate suppressed responses but oddball responses are large and distinct. Oscillatory mismatch responses persist in population activity for long periods after stimulus offset while individual cell mismatch responses are strongly phasic. These effects are weakened in temporally irregular sensory streams. Thus we show that network phase entrainment provides a biologically plausible mechanism for neural oddball detection. Our results do not depend on specific network characteristics, are consistent with experimental studies and may be relevant for multiple pathologies demonstrating altered mismatch processing such as schizophrenia and depression.

Highlights

  • In predictably structured sensory streams like music, speech and visual input during motion the brain doesn’t respond to external events but anticipates them[1,2,3,4]

  • Type expectation occurs at the neuronal population level as oscillatory mismatch responses (MMR) after stimulus offset in EEG/MEG23–27, ECoG19, and LFP28

  • Unstructured recurrent networks generate fairly low dimensional chaotic dynamics. We show that this is because entrainment of chaotic oscillations[63] results in the complex close to critical dynamics[64,65] which supports the history dependent response on long behaviourally relevant timescales necessary for sensory stream adaptation[66,67]

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Summary

Introduction

In predictably structured sensory streams like music, speech and visual input during motion the brain doesn’t respond to external events but anticipates them[1,2,3,4]. The sensory streams used are found to phase entrain low-frequency brain oscillations[9,10,11,12]. SSA is thought to depend on single cell adaptation but studies have implicated network mechanisms[21,40,41] including recurrent inhibition[42,43]. Unstructured recurrent networks generate fairly low dimensional chaotic dynamics We show that this is because entrainment of chaotic oscillations[63] results in the complex close to critical dynamics[64,65] which supports the history dependent response on long behaviourally relevant timescales necessary for sensory stream adaptation[66,67]

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