Multiplexed and Robust Representations of Sound Features in Auditory Cortex

Abstract

We can recognize the melody of a familiar song when it is played on different musical instruments. Similarly, an animal must be able to recognize a warning call whether the caller has a high-pitched female or a lower-pitched male voice, and whether they are sitting in a tree to the left or right. This type of perceptual invariance to "nuisance" parameters comes easily to listeners, but it is unknown whether or how such robust representations of sounds are formed at the level of sensory cortex. In this study, we investigate whether neurons in both core and belt areas of ferret auditory cortex can robustly represent the pitch, formant frequencies, or azimuthal location of artificial vowel sounds while the other two attributes vary. We found that the spike rates of the majority of cortical neurons that are driven by artificial vowels carry robust representations of these features, but the most informative temporal response windows differ from neuron to neuron and across five auditory cortical fields. Furthermore, individual neurons can represent multiple features of sounds unambiguously by independently modulating their spike rates within distinct time windows. Such multiplexing may be critical to identifying sounds that vary along more than one perceptual dimension. Finally, we observed that formant information is encoded in cortex earlier than pitch information, and we show that this time course matches ferrets' behavioral reaction time differences on a change detection task.

Neural processing of natural sounds

“…formant frequency) that are robust to variation in other physical parameters of the sound (e.g. azimuthal location) and such responses have been found in secondary mammalian and avian auditory areas [91,92]. In terms of higher-level categorization, research in starlings points to a role of the Caudio-Medial Nidopallium (NCM) for classifying behaviorally relevant classes of songs [93] and research in primates suggests that both the Superior Temporal Gyrus (STG) and the ventrolateral Prefontral Cortex (vPFC) could be involved in semantic discrimination [94][95][96][97][98].…”

Six Degrees of Auditory Spatial Separation

“…Indeed, the available cortical and imaging data indicates it is not (King and Middlebrooks 2010;Ahveninen et al 2014) and could be based instead on a logical representation of space operating as a network of neural interconnections. The temporally complex and integrative nature of auditory cortical processing (Walker et al 2011;Bizley and Cohen 2013) and the need to integrate nonauditory cues (e.g., Goossens and van Opstal 1999) suggests that auditory space and the objects within it will ultimately depend on diverse inputs. Importantly, our stimuli were two spectro-temporally complex stimuli chosen so that their various components would strongly bind to one of two perceptual objects.…”

Cortico‐cortical connectivity within ferret auditory cortex

“…The presence of multiple auditory cortical areas on the ectosylvian gyrus (EG) of this species was first demonstrated by using 2‐deoxyglucose autoradiography (Wallace et al, 1997) and subsequently confirmed by using optical imaging of intrinsic signals (Nelken et al, 2004) and single‐unit recording (Kelly et al, 1986; Kelly and Judge, 1994; Kowalski et al, 1995; Bizley et al, 2005). Although most electrophysiological recording studies have focused on the primary auditory cortex (A1) (Phillips et al, 1988; Kowalski et al, 1996; Schnupp et al, 2001; Fritz et al, 2003; Rabinowitz et al, 2011; Keating et al, 2013), the nonprimary auditory fields in this species are now receiving increasing attention (Nelken et al, 2008; Bizley et al, 2009, 2010, 2013; Walker et al, 2011; Atiani et al, 2014). …”