Effects of Auditory Stimulus Context on the Representation of Frequency in the Gerbil Inferior Colliculus

Abstract

Prior studies of dynamic conditioning have focused on modulation of binaural localization cues, revealing that the responses of inferior colliculus (IC) neurons to particular values of interaural phase and level disparities depend critically on the context in which they occur. Here we show that monaural frequency transitions, which do not simulate azimuthal motion, also condition the responses of IC neurons. We characterized single-unit responses to two frequency transition stimuli: a glide stimulus comprising two tones linked by a linear frequency sweep (origin-sweep-target) and a step stimulus consisting of one tone followed immediately by another (origin-target). Using sets of glide and step stimuli converging on a common target, we constructed conditioned response functions (RFs) depicting the variability in the response to an identical stimulus as a function of the preceding origin frequency. For nearly all cells, the response to the target depended on the origin frequency, even for origins outside the excitatory frequency response area of the cell. Results from conditioned RFs based on long (2–4 s) and short (200 ms) duration step stimuli indicate that conditioning effects can be induced in the absence of the dynamic sweep, and by stimuli of relatively short duration. Because IC neurons are tuned to frequency, changes in the origin frequency often change the “effective” stimulus duty cycle. In many cases, the enhancement of the target response appeared related to the decrease in the “effective” stimulus duty cycle rather than to the prior presentation of a particular origin frequency. Although this implies that nonselective adaptive mechanisms are responsible for conditioned responses, slightly more than half of IC neurons in each paradigm responded significantly differently to targets following origins that elicited statistically indistinguishable responses. The prevailing influence of stimulus context when discharge history is controlled demonstrates that not all the mechanisms governing conditioning depend on the discharge history of the recorded neuron. Selective adaptation among the neuron's variously tuned afferents may help engender stimulus-specific conditioning. The demonstration that conditioning effects reflect sensitivity to spectral as well as spatial stimulus contrast has broad implications for the processing of a wide range of dynamic acoustic signals and sound sequences.