Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus

In many neural systems studied in vitro, the timing of afferent impulses affects the strength of postsynaptic potentials1,2. The influence of afferent timing on postsynaptic firing in vivo has received less attention. Here we study the importance of afferent spike timing in vivo by recording simultaneously from ganglion cells in the retina and their targets in the lateral geniculate nucleus of the thalamus. When two spikes from a single ganglion-cell axon arrive within 30 milliseconds of each other, the second spike is much more likely than the first to produce a geniculate spike, an effect we call paired-spike enhancement. Furthermore, simultaneous recordings from a ganglion cell and two thalamic targets indicate that paired-spike enhancement increases the frequency of synchronous thalamic activity. We propose that information encoded in the high firing rate of an individual retinal ganglion cell becomes distributed among several geniculate neurons that fire synchronously. Because synchronous geniculate action potentials are highly effective in driving cortical neurons3, it is likely that information encoded by this strategy is transmitted to the next level of processing.