Contribution of spike timing to the information transmitted by HVC neurons

In many species, neurons with highly selective stimulus-response properties characterize higher order sensory areas and/or sensory motor areas of the CNS. In the songbird nuclei, the responses of HVC (used as a proper name) neurons during playback of the bird's own song (BOS) are probably one of the most striking examples of selectivity for natural stimuli. We examined here to what extent spike-timing carries information about natural and time-reversed versions of the BOS. From a heterogenous population of 107 HVC neurons recorded in long-day or short-day conditions, a standard indicator of stimulus preference based on spike-count (the d' index) indicates that a limited proportion of cells can be classified as selective for the BOS (20% with a vertical bar d vertical bar > 1). In contrast, quantifying the information conveyed by spike trains with the metric-space of J. D. Victor & K. P Purpura [(1996) J. Neurophysiol., 76, 1310 - 1326] indicates that 62% of the cells display significant amounts of transmitted information, among which 77% are 'temporal cells'. 'Temporal cells' correspond to cells transmitting significant amounts of information when spike-timing is considered, whereas no information, or lower amounts of transmitted information, is obtained when only spike-count is considered. Computing a correlation index between spike trains [S. Schreiber et al. (2003) Neurocomputing, 52-54,925-931] revealed that spike-timing reliability is higher for the forward than for the reverse BOS, whatever the day length and the cell type are. Cells classified as selective in terms of spike-counts (d' index) had greater amounts of transmitted information, but cells classified as non-selective (d' < 0.5) can also transmit significant amounts of information. Thus, information theory methods demonstrate that a much larger proportion of neurons than expected based on spike-count only participate in the discrimination between stimuli.