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Synchronous spikes are necessary but not sufficient for a synchrony code in populations of spiking neurons

Significance Populations of sensory neurons convey information about the outside world to the brain. Postsynaptic neurons may read out their total activity or, alternatively, by focusing only on synchronous activity, they might extract specific features from the same sensory information. But does synchronous activity always encode special features of the stimulus? This question was experimentally addressed in in vivo recordings from two closely related populations of electrosensory neurons of a weakly electric fish. Despite having similar amounts of synchronous activity, only in one population of neurons did synchronous spikes carry specific information about the stimulus. A detailed spectral analysis reveals that too low levels of intrinsic noise paired with too little frequency locking of the neural oscillator destroys a synchrony code. Synchronous activity in populations of neurons potentially encodes special stimulus features. Selective readout of either synchronous or asynchronous activity allows formation of two streams of information processing. Theoretical work predicts that such a synchrony code is a fundamental feature of populations of spiking neurons if they operate in specific noise and stimulus regimes. Here we experimentally test the theoretical predictions by quantifying and comparing neuronal response properties in tuberous and ampullary electroreceptor afferents of the weakly electric fish Apteronotus leptorhynchus. These related systems show similar levels of synchronous activity, but only in the more irregularly firing tuberous afferents a synchrony code is established, whereas in the more regularly firing ampullary afferents it is not. The mere existence of synchronous activity is thus not sufficient for a synchrony code. Single-cell features such as the irregularity of spiking and the frequency dependence of the neuron’s transfer function determine whether synchronous spikes possess a distinct meaning for the encoding of time-dependent signals.