A Spike-Timing Code for Discriminating Conspecific Vocalizations in the Thalamocortical System of Anesthetized and Awake Guinea Pigs

Understanding how communication sounds are processed and encoded in the central auditory system is critical to understanding the neural bases of acoustic communication. Here, we examined neuronal representations of species-specific vocalizations, which are communication sounds that many species rely on for survival and social interaction. In some species, the evoked responses of auditory cortex neurons are stronger in response to natural conspecific vocalizations than to their time-reversed, spectrally identical, counterparts. We applied information theory-based analyses to single-unit spike trains collected in the auditory cortex (n = 139) and auditory thalamus (n = 135) of anesthetized animals as well as in the auditory cortex (n = 119) of awake guinea pigs during presentation of four conspecific vocalizations. Few thalamic and cortical cells (<10%) displayed a firing rate preference for the natural version of these vocalizations. In contrast, when the information transmitted by the spike trains was quantified with a temporal precision of 10-50 ms, many cells (>75%) displayed a significant amount of information (i.e., >2SD above chance levels), especially in the awake condition. The computed correlation index between spike trains (R-corr, defined by Schreiber et al., 2003) indicated similar spike-timing reliability for both the natural and time-reversed versions of each vocalization, but higher reliability for awake animals compared with anesthetized animals. Based on temporal discharge patterns, even cells that were only weakly responsive to vocalizations displayed a significant level of information. These findings emphasize the importance of temporal discharge patterns as a coding mechanism for natural communication sounds, particularly in awake animals.