Enhancement in the Marmoset Inferior Colliculus: Neural Correlates of Perceptual “Pop-Out”

Abstract

Although new information about external stimuli cannot be generated centrally, it is clear that the auditory system can selectively suppress or enhance different features of the peripheral response to acoustic stimulation. One example is the robust perceptual “pop out” of a single component within a broadband sound whose onset time is delayed relative to the remainder of the complex. Single auditory nerve fibers do not exhibit enhanced responses using such stimuli (J Acoust Soc Am 97:1786-1799, 1995); the percept is presumably derived from the amplification in the central auditory system of some set of features within the population peripheral response. The goals of this study were (1) to determine whether this neural integration occurs at or below the inferior colliculus (IC), and (2) to compare the effects of specific stimuli and parameter variations between physiological and psychophysical experiments. Single-unit activity was recorded in the IC of the awake marmoset in response to stimuli loosely modeled after previous behavioral and physiological studies of the enhancement effect. A 100-ms best-frequency (BF) tone was presented within a wideband sound with a spectral notch centered on BF. In many IC neurons, responses were significantly larger to this stimulus when a 500-ms preceding signal consisting of the band-reject complex was presented than when silence was presented prior to the probe.

Appendices

Comment by Skyler Jennings

Viemeister and Bacon (1982) proposed “adaptation of suppression” as an explanation of enhancement. In the discussion of the same paper, they suggest this adaptation may exist in the auditory periphery when they state: “Although adaptation of suppression is not seen peripherally, preliminary psychophysical data from our laboratory are not incompatible with this notion...”

The straightforward interpretation of the data presented in the current study does not support the idea that adaptation of suppression occurred in the auditory periphery. Presumably, this is because previous studies in the auditory nerve (AN) and cochlear nucleus (CN) did not show enhancement. However, one notable difference between your study and the studies in the AN and CN is the fact that your data come from awake animals. Is it possible that adaptation of suppression is mediated peripherally by the olivocochlear efferents, but enhancement was not seen in the AN and CN due to the effects of anesthesia on the efferent system?

Reply by Paul Nelson

While we cannot rule out the possible influence of efferent activity, it seems unlikely that the entire effect is generated via an anesthetic-sensitive component of the olivocochlear system. First, the unpublished CN data (Scutt 2000) that were collected using the same animal and anesthesia regiment as the AN study (Palmer et al. 1995) did show modest enhancement in some neurons. This suggests that low-level central processing can produce the effect, but it does not directly address the question of how the ascending representation might differ in our awake preparation. The only way to unequivocally rule out a direct peripheral influence on IC enhancement would be to record from AN fibers in unanesthetized marmosets.

Attentional effects are also commonly linked to olivocochlear influences. The animals in this study were passively listening to the stimuli (i.e., their attention was not controlled). If the olivocochlear system influence is attention-modulated and responsible for the response facilitation, one might expect that an active listening task would be required before enhancement would be reflected in responses of single neurons. We speculate that a more automatic set of central processes underlies the phenomenon at the level of the IC.