Responses of neurons in the marmoset primary auditory cortex to interaural level differences: comparison of pure tones and vocalizations.

Leo L Lui,Yasamin Mokri,Ramesh Rajan,David H Reser,Marcello G P Rosa

doi:10.3389/fnins.2015.00132

Abstract

Interaural level differences (ILDs) are the dominant cue for localizing the sources of high frequency sounds that differ in azimuth. Neurons in the primary auditory cortex (A1) respond differentially to ILDs of simple stimuli such as tones and noise bands, but the extent to which this applies to complex natural sounds, such as vocalizations, is not known. In sufentanil/N2O anesthetized marmosets, we compared the responses of 76 A1 neurons to three vocalizations (Ock, Tsik, and Twitter) and pure tones at cells' characteristic frequency. Each stimulus was presented with ILDs ranging from 20 dB favoring the contralateral ear to 20 dB favoring the ipsilateral ear to cover most of the frontal azimuthal space. The response to each stimulus was tested at three average binaural levels (ABLs). Most neurons were sensitive to ILDs of vocalizations and pure tones. For all stimuli, the majority of cells had monotonic ILD sensitivity functions favoring the contralateral ear, but we also observed ILD sensitivity functions that peaked near the midline and functions favoring the ipsilateral ear. Representation of ILD in A1 was better for pure tones and the Ock vocalization in comparison to the Tsik and Twitter calls; this was reflected by higher discrimination indices and greater modulation ranges. ILD sensitivity was heavily dependent on ABL: changes in ABL by ±20 dB SPL from the optimal level for ILD sensitivity led to significant decreases in ILD sensitivity for all stimuli, although ILD sensitivity to pure tones and Ock calls was most robust to such ABL changes. Our results demonstrate differences in ILD coding for pure tones and vocalizations, showing that ILD sensitivity in A1 to complex sounds cannot be simply extrapolated from that to pure tones. They also show A1 neurons do not show level-invariant representation of ILD, suggesting that such a representation of auditory space is likely to require population coding, and further processing at subsequent hierarchical stages.

Highlights

The number of cells sensitive to Interaural level differences (ILDs) is shown in Table 1, and this depended on stimulus type [χ2(3) = 9.23, P = 0.026]: more cells were sensitive to the Ock (77%) and the appropriate characteristic frequencies (CFs) tone (78%) compared to the number of cells sensitive to the Tsik (63%) and Twitter (69%)
The majority of the ILD-sensitive cells had monotonic response functions with a strong bias toward the side from which stronger responses were elicited. This was obviously true of the ILDs that elicited the maximum firing rate in each cell, but we found this bias in the midpoints of the ILD-response functions, which tended to be displaced toward the ear eliciting the stronger responses
Other investigators have reported compatible results: while spatial receptive field sizes may change with increasing level, the positive and negative changes offset each other, which equated to no significant changes in receptive size (Mickey and Middlebrooks, 2003; Woods et al, 2006; Zhou and Wang, 2012). The latter studies were conducted in awake animals, we have shown that our opiate anesthetic regime yields auditory cortical recordings that are more comparable to those described for awake animals, at least in early hierarchical stages of processing such as A1 (Rajan et al, 2013)

Summary

Introduction

The mammalian primary auditory cortex (A1) is critical for sound localization (Thompson and Cortez, 1983; Jenkins and Merzenich, 1984; Heffner and Heffner, 1990), and the responses of single A1 neurons encode information about sound source locations (e.g., Phillips and Irvine, 1981, 1983; Rajan et al, 1990; Recanzone et al, 2000; Mrsic-Flogel et al, 2005; Woods et al, 2006; Kusmierek and Rauscheker, 2014; see Grothe et al, 2010 for review). The spatial sensitivity of A1 neurons can vary with stimulus level (e.g., Brugge et al, 1996; Middlebrooks et al, 1998; Reale et al, 2003; Zhou and Wang, 2012). The social behavior of marmoset monkeys requires a range of context-specific vocalizations (Stevenson and Poole, 1976) These provide auditory stimuli that are both complex and biologically relevant (Miller et al, 2009), which have become the focus of many studies (i.e., Lu et al, 2001; Nagarajan et al, 2002; Eliades and Wang, 2003, 2013). The spatial receptive fields in response noise-bands have been well characterized in marmoset A1 (Zhou and Wang, 2012, 2014), stimulus driven responses to complex stimuli may not necessarily reflect those elicited by noise bands and pure tones, given that nonlinear spectrotemporal interactions underlie A1 neuronal responses (Sadagopan and Wang, 2009)

Results

Discussion

Conclusion