Nonlinear Spectrotemporal Interactions Underlying Selectivity for Complex Sounds in Auditory Cortex

Sadagopan and Wang demonstrate that neurons in marmoset auditory cortex display combination sensitivity that underlies responsiveness to complex sounds. This work reinforces evidence of continuity in processing of complex sounds across a range of mammals and other vertebrates. My comments relate to the article’s proposal that combination sensitivity in marmoset cortex is likely the result of interactions that occur in auditory cortex, especially in its upper layers. In bats and mice, there is now clear evidence that combination-sensitive responses originate at levels below auditory cortex. The issue is particularly relevant to our understanding of the mechanisms that create such interesting response properties.

A wide diversity of combination-sensitive responses occurs in the inferior colliculus (IC) of bats and other mammals, characterized by facilitated responses to tone or noise combinations. The frequency combinations can be separated by a few kilohertz or several octaves. The temporal sensitivity can be on a sub-millisecond scale or on a scale of tens of milliseconds, and often does not depend on the duration of the facilitating sounds. Thus, in each of these features, combination sensitivity observed in the marmoset cortex is similar to that observed in the IC of bats and mice (Mittmann and Wenstrup, 1995; Yan and Suga, 1996; Portfors and Wenstrup, 1999; Leroy and Wenstrup, 2000; Nataraj and Wenstrup, 2005; Portfors and Felix, 2005; Gans et al., 2009).

Concerning mechanisms, work in the mustached bat shows that the interactions underlying combination-sensitive facilitation arise through differently tuned glycinergic inputs onto IC neurons. Interestingly, glutamatergic inputs do not appear to play a role in the facilitation, even though they mediate responses to single tonal stimuli in the same neurons (Wenstrup and Leroy, 2001; Nataraj and Wenstrup, 2005; Sanchez et al., 2008).

While this article proposes that combination sensitivity arises via cortical processing, the available evidence suggests that such interactions likely originate in the IC. Things may be different in the marmoset, but, given the similarity to response features in other mammals, there is no a priori reason to make that assumption. Instead, I suggest that the combination sensitivity originating in the IC becomes more apparent as subsequent processing suppresses the responses to single tonal stimuli.

REFERENCES

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Nataraj K, Wenstrup JJ (2005) Roles of inhibition in creating complex auditory responses in the inferior colliculus: facilitated combination-sensitive neurons. J Neurophysiol 93:3294-3312.

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