Hypotheses of sensory coding range from the notion of nonlinear "feature detectors" to linear rate coding strategies. Here, we report that auditory neurons exhibit a novel trade-off in the relationship between sound selectivity and the information that can be communicated to a postsynaptic cell. Recordings from the cat inferior colliculus show that neurons with the lowest spike rates reliably signal the occurrence of stereotyped stimulus features, whereas those with high response rates exhibit lower selectivity. The highest information conveyed by individual action potentials comes from neurons with low spike rate and high selectivity. Surprisingly, spike information is inversely related to spike rates, following a trend similar to that of feature selectivity. Information per time interval, however, was proportional to measured spike rates. A neuronal model based on the spike threshold of the synaptic drive accurately accounts for this trade-off: higher thresholds enhance the spiking fidelity at the expense of limiting the total communicated information. Such a constraint on the specificity and throughput creates a continuum in the neural code with two extreme forms of information transfer that likely serve complementary roles in the representation of the auditory environment.

Binaural disparities are the primary acoustic cues employed in sound localization tasks. However, the degree of binaural correlation in a sound serves as a complementary cue for detecting competing sound sources [J. F. Culling, H. S. Colburn, and M. Spurchise, “Interaural correlation sensitivity,” J. Acoust. Soc. Am. 110(2), 1020–1029 (2001) and L. R. Bernstein and C. Trahiotis, “On the use of the normalized correlation as an index of interaural envelope correlation,” J. Acoust. Soc. Am. 100, 1754–1763 (1996)]. Here a random chord stereogram (RCS) sound is developed that produces a salient pop-out illusion of a slowly varying ripple sound [T. Chi et al., “Spectro-temporal modulation transfer functions and speech intelligibility,” J. Acoust. Soc. Am. 106(5), 2719–2732 (1999)], even though the left and right ear sounds alone consist of noise-like random modulations. The quality and resolution of this percept is systematically controlled by adjusting the spectrotemporal correlation pattern between the left and right sounds. The prominence and limited time-frequency resolution for resolving the RCS suggests that envelope correlations are a dominant binaural cue for grouping acoustic objects.