Neural dynamics in a model of the thalamocortical system. II. The role of neural synchrony tested through perturbations of spike timing.

Activity in the mammalian thalamocortical system is often accompanied by a synchronous discharge of cortical and thalamic neurons. Although many functions have been attributed to such synchronous firing, it is not known whether or how synchrony of firing per se affects thalamocortical operations. Direct experimental tests of the consequences of neuronal synchronization in vivo are hard to carry out, whereas theoretical studies based on single-neuron models cannot reveal the effects of synchrony at the system level. To overcome these limitations, we have used a perturbational approach to test the causal efficacy of synchrony per se in large-scale simulations of the thalamocortical system. The test consists of selectively disrupting firing synchrony by 'jittering' the timing of action potentials in the simulations and determining whether firing rates are modified by this perturbation. The simulations are based in detail on the known anatomy and physiology of the thalamocortical-visual system of the cat, and have been shown in a companion paper to produce episodes of fast synchronous activity at multiple levels. By carrying out the perturbation analysis, we established that neurons can have long membrane time constants (8-16 ms) and balanced synaptic activations, and yet function collectively in such a way that synchrony within a time window of 4 ms significantly affects the rates and selectivity of the responses to visual stimuli. The simulations also revealed a complex interplay, at the network level, between synchrony of firing and rate of firing. The dynamic consequences of firing synchrony were most evident when spike jittering was applied to specific polysynaptic loops involving corticocortical and corticothalamic connections. These results support the view that firing synchrony within thalamocortical and corticocortical loops plays a causal role in the cooperative and competitive neural interactions that produce pattern-selective responses in the cortex.