Amplitude and direction of saccadic eye movements depend on the synchronicity of collicular population activity

Synchronization of neuronal discharges has been observed in numerous brain structures, but opinions diverge regarding its significance in neuronal processing. Here we investigate whether the motion vectors of saccadic eye movements evoked by electrical multisite stimulation of the cat superior colliculus (SC) are influenced by varying the degree of synchrony between the stimulus trains. With synchronous activation of SC sites, the vectors of the resulting saccades correspond approximately to the averages of the vectors of saccades evoked from each site alone. In contrast, when the pulses of trains applied to the different sites are temporally offset by as little as 5-10 ms, the vectors of the resulting saccades come close to the sum of the individual vectors. Thus saccade vectors depend not only on the site and amplitude of collicular activation but also on the precise temporal relations among the respective spike trains. These data indicate that networks within or downstream from the SC discriminate with high temporal resolution between synchronous and asynchronous population responses. This supports the hypothesis that information is encoded not only in the rate of neuronal responses but also in the precise temporal relations between discharges.