Sound frequency representation in primary auditory cortex is level tolerant for moderately loud, complex sounds

Abstract

Pienkowski M, Eggermont JJ. Sound frequency representation in primary auditory cortex is level tolerant for moderately loud, complex sounds. J Neurophysiol 106: 1016 -1027, 2011. First published June 8, 2011 doi:10.1152/jn.00291.2011The distribution of neuronal characteristic frequencies over the area of primary auditory cortex (AI) roughly reflects the tonotopic organization of the cochlea. However, because the area of AI activated by any given sound frequency increases erratically with sound level, it has generally been proposed that frequency is represented in AI not with a rate-place code but with some more complex, distributed code. Here, on the basis of both spike and local field potential (LFP) recordings in the anesthetized cat, we show that the tonotopic representation in AI is much more level tolerant when mapped with spectrotemporally dense tone pip ensembles rather than with individually presented tone pips. That is, we show that the tuning properties of individual unit and LFP responses are less variable with sound level under dense compared with sparse stimulation, and that the spatial frequency resolution achieved by the AI neural population at moderate stimulus levels (65 dB SPL) is better with densely than with sparsely presented sounds. This implies that nonlinear processing in the central auditory system can compensate (in part) for the level-dependent coding of sound frequency in the cochlea, and suggests that there may be a functional role for the cortical tonotopic map in the representation of complex sounds. multiunit spikes; local field potentials; spectrotemporal receptive fields; tuning curves THE LARGE-SCALE TONOTOPIC organization of mammalian primary auditory cortex (AI) is well-established (e.g., Humphries et al. 2010;Merzenich et al. 1975;Reale and Imig 1980;Woolsey 1972), at least for the population of layer III and IV pyramidal cells, which receive afferent input from the principal neurons of the ventral nucleus of the medial geniculate body (MGB), the primary nucleus of the lemniscal auditory pathway (Winer 1992). In other words, the distribution of neuronal characteristic frequencies (CFs; best frequencies at response threshold) over the area of layer III/IV reflects the orderly place code for sound frequency established mechanoelectrically in the cochlea. A pair of recent in vivo two-photon calcium imaging studies have indicated that, at the level of wellisolated units of presumably various cell types in layers II and III, the distribution of CFs appears more disordered on small distance scales (Bandyopadhyay et al. 2010;Rothschild et al. 2010). Thus more superficial layers of AI exhibit a more coarse tonotopy, a fact not entirely unexpected given the extensive frequency integration that occurs in AI (Happel et al. 2010;Imaizumi and Schreiner 2007;Kaur et al. 2004;Read et al. 2001;Schreiner et al. 2000;Wallace et al. 1991;Winer 1992).The CF distribution, by itself, gives only limited insight into the spatial representation of sound frequency in AI. As stated by Phillips et al....

Component analysis reveals sharp tuning of the local field potential in the guinea pig auditory cortex

“…than high intensities, at least for spectrally sparse stimuli (Galván et al 2001;Pienkowski and Eggermont 2011).…”

Compensating Level-Dependent Frequency Representation in Auditory Cortex by Synaptic Integration of Corticocortical Input

“…Interestingly, Pienkowski and Eggermont (2011) have reported a level-invariant representation of the spectral energy of acoustic stimuli based on MUA and LFP signals only for responses to complex sounds, but not for single tone pips, as used in this study [74]. Due to the spectral energy distribution of complex tones it has been suggested that competitive interactions between cortical columns account for the spectral integration [14,75].…”

A Review of Hyperacusis and Future Directions: Part II. Measurement, Mechanisms, and Treatment

“…Thus, by the level of auditory cortex, complex sounds may be represented in a largely intensity-independent, "object-oriented" fashion (Billimoria, Kraus, Narayan, Maddox, & Sen, 2008;Pienkowski & Eggermont, 2011c; for a review, see Barbour, 2011), particularly during attentive listening (Ding & Simon, 2012;Mesgarani & Chang, 2012), although the basis for such representations may begin to emerge in the cochlear nucleus (Blackburn & Sachs, 1990; for a review, see Young, 1998). Thus, by the level of auditory cortex, complex sounds may be represented in a largely intensity-independent, "object-oriented" fashion (Billimoria, Kraus, Narayan, Maddox, & Sen, 2008;Pienkowski & Eggermont, 2011c; for a review, see Barbour, 2011), particularly during attentive listening (Ding & Simon, 2012;Mesgarani & Chang, 2012), although the basis for such representations may begin to emerge in the cochlear nucleus (Blackburn & Sachs, 1990; for a review, see Young, 1998).…”