Who reads temporal information contained across synchronized and oscillatory spike trains?

Abstract

Our inferences about brain mechanisms underlying perception rely on whether it is possible for the brain to ‘reconstruct’ a stimulus from the information contained in the spike trains from many neurons^1,2,3,4,5. How the brain actually accomplishes this reconstruction remains largely unknown. Oscillatory and synchronized activities in the brain of mammals have been correlated with distinct behavioural states or the execution of complex cognitive tasks^{6,7,8,9,10,11} and are proposed to participate in the ‘binding’ of individual features into more complex percepts^12,13,14,. But if synchronization is indeed relevant, what senses it? In insects, oscillatory synchronized activity in the early olfactory system seems to be necessary for fine odour discrimination¹⁵ and enables the encoding of information about a stimulus in spike times relative to the oscillatory ‘clock’¹⁶. Here we study the decoding of these coherent oscillatory signals. We identify a population of neurons downstream from the odour-activated, synchronized neuronal assemblies. These downstream neurons show odour responses whose specificity is degraded when their inputs are desynchronized. This degradation of selectivity consists of the appearance of responses to new odours and a loss ofdiscrimination of spike trains evoked by different odours. Suchloss of information is never observed in the upstream neurons whose activity is desynchronized. These results indicate that information encoded in time across ensembles of neurons converges onto single neurons downstream in the pathway.