Spike timing and the coding of naturalistic sounds in a central auditory area of songbirds

In nature, animals encounter high dimensional sensory stimuli that have complex statistical and dynamical structure. Attempts to study the neural coding of these natural signals face challenges both in the selection of the signal ensemble and in the analysis of the resulting neural responses. For zebra finches, naturalistic stimuli can be defined as sounds that they encounter in a colony of conspecific birds. We assembled an ensemble of these sounds by recording groups of 10-40 zebra finches, and then analyzed the response of single neurons in the songbird central auditory area (field L) to continuous playback of long segments from this ensemble. Following methods developed in the fly visual system, we measured the information that spike trains provide about the acoustic stimulus without any assumptions about which features of the stimulus are relevant. Preliminary results indicate that large amounts of information are carried by spike timing, with roughly half of the information accessible only at time resolutions better than 10 ms; additional information is still being revealed as time resolution is improved to 2 ms. Information can be decomposed into that carried by the locking of individual spikes to the stimulus (or modulations of spike rate) vs. that carried by timing in spike patterns. Initial results show that in field L, temporal patterns give at least 20% extra information. Thus, single central auditory neurons can provide an informative representation of naturalistic sounds, in which spike timing may play a significant role.