Neural Synchrony Gives Rise to Amplitude- and Duration-Invariant Encoding Consistent With Perception of Natural Communication Stimuli

Abstract

When confronted with a highly variable environment, it remains poorly understood how neural populations encode and classify natural stimuli to give rise to appropriate and consistent behavioral responses. Here we investigated population coding of natural communication signals with different attributes (i.e., amplitude and duration) in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus. Our results show that, while single peripheral neurons encode the detailed timecourse of different stimulus waveforms, measures of population synchrony are effectively unchanged because of coordinated increases and decreases in activity. A phenomenological mathematical model reproduced this invariance and shows that this can be explained by considering homogeneous populations whose responses are solely determined by single neuron firing properties. Moreover, recordings from downstream central neurons reveal that synchronous afferent activity is actually decoded and thus most likely transmitted to higher brain areas. Finally, we demonstrate that the associated behavioral responses at the organism level are invariant. Our results provide a mechanism by which amplitude- and duration-invariant coding of behaviorally relevant sensory input emerges across successive brain areas thereby presumably giving rise to invariant behavioral responses. Such mechanisms are likely to be found in other systems that share anatomical and functional features with the electrosensory system (e.g., auditory, visual, vestibular).