Contribution of spike timing to the information transmitted by HVC neurons

Abstract

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 |d'| > 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.

What can spike train distances tell us about the neural code?

“…This is because I * (S P , S; τ ) can have piecewise constant intervals (e. g. Victor and Purpura, 1996;Di Lorenzo and Victor, 2003;Roussin et al, 2008;Huetz et al, 2006Huetz et al, , 2009. Different criteria have been chosen in experimental studies that apply the discrimination analysis, but often there is not an explicit explanation of how to calculate τ * .…”

“…Different criteria have been chosen in experimental studies that apply the discrimination analysis, but often there is not an explicit explanation of how to calculate τ * . In Huetz et al (2006) and Wohlgemuth and Ronacher (2007), the average of τ is taken when a plateau is obtained. In Roussin et al (2008) they comment that the influence of temporal coding may be underestimated because they consider as rate coding any case in which I * max (S P , S) is obtained for τ = ∞, even if lower time scales provide the same information.…”

“…For D V we have chosen τ V = 2 q . This selection has been used in several previous studies (Victor and Purpura, 1996;Reich et al, 2001b;Huetz et al, 2009), but it is also common to use τ V = 1 q (e. g. Victor and Purpura, 1997;Samonds and Bonds, 2004;Huetz et al, 2006). Notice that, although for an individual pair of spikes 2/q corresponds to the maximum time shift allowed, for complete spike trains τ V = 2/q does not indicate the time scale of the time shifts actually used in the minimal cost transformation.…”

Statistical Analyses of Temporal Information in Auditory Brainstem Responses to Tones in Noise: Correlation Index and Spike-distance Metric

“…In previous auditory studies ( Chase and Young 2006;Huetz et al 2006), the temporal resolution that yields the maximum mutual information has been identified as the time scale most likely used by a certain auditory stage when processing temporal information. The present study showed that the best temporal resolution, determined by q, can be biased toward low values by variations in average rate.…”

“…The mutual information quantified by the spike-distance metric indicates the efficiency of spike timing in coding the stimuli at different temporal resolutions. Although Victor and Purpura (1997) state that this approach may not incorporate all types of temporal information as an optimal temporal measure, this approach has been used in recent auditory studies as a general evaluation of the contribution of temporal information compared to that of average rate (Chase and Young 2006;Edeline 2004/2005;Huetz et al 2006). In the present study, the spike-distance metric was compared to other temporal measures for tone-innoise responses.…”