Long-lasting modulation by stimulus context in primate auditory cortex.

Abstract

A sound embedded in an acoustic stream cannot be unambiguously segmented and identified without reference to its stimulus context. To understand the role of stimulus context in cortical processing, we investigated the responses of auditory cortical neurons to 2-sound sequences in awake marmosets, with a focus on stimulus properties other than carrier frequency. Both suppressive and facilitatory modulations of cortical responses were observed by using combinations of modulated tone and noise stimuli. The main findings are as follows. 1) Preceding stimuli could suppress or facilitate responses to succeeding stimuli for durations >1 s. These long-lasting effects were dependent on the duration, sound level, and modulation parameters of the preceding stimulus, in addition to the carrier frequency. They occurred regardless of whether the 2 stimuli were separated by a silent interval. 2) Suppression was often tuned such that preceding stimuli whose parameters were similar to succeeding stimuli produced the strongest suppression. However, the responses of many units could be suppressed, although often weaker, even when the 2 stimuli were dissimilar. In some cases, only a dissimilar preceding stimulus produced suppression in the responses to the succeeding stimulus. 3) In contrast to suppression, facilitation of responses to succeeding stimuli by the preceding stimulus was usually strongest when the 2 stimuli were dissimilar. 4) There was no clear correlation between the firing rate evoked by the preceding stimulus and the change in the firing rate evoked by the succeeding stimulus, indicating that the observed suppression was not simply a result of habituation or spike adaptation. These results demonstrate that persistent modulations of the responses of an auditory cortical neuron to a given stimulus can be induced by preceding stimuli. Decreases or increases of responses to the succeeding stimuli are dependent on the spectral, temporal, and intensity properties of the preceding stimulus. This indicates that cortical auditory responses to a sound are not static, but instead depend on the stimulus context in a stimulus-specific manner. The long-lasting impact of stimulus context and the prevalence of facilitation suggest that such cortical response properties are important for auditory processing beyond forward masking, such as for auditory streaming and segregation.