Interdependent Encoding of Pitch, Timbre, and Spatial Location in Auditory Cortex

Abstract

Because we can perceive the pitch, timbre, and spatial location of a sound source independently, it seems natural to suppose that cortical processing of sounds might separate out spatial from nonspatial attributes. Indeed, recent studies support the existence of anatomically segregated "what" and "where" cortical processing streams. However, few attempts have been made to measure the responses of individual neurons in different cortical fields to sounds that vary simultaneously across spatial and nonspatial dimensions. We recorded responses to artificial vowels presented in virtual acoustic space to investigate the representations of pitch, timbre, and sound source azimuth in both core and belt areas of ferret auditory cortex. A variance decomposition technique was used to quantify the way in which altering each parameter changed neural responses. Most units were sensitive to two or more of these stimulus attributes. Although indicating that neural encoding of pitch, location, and timbre cues is distributed across auditory cortex, significant differences in average neuronal sensitivity were observed across cortical areas and depths, which could form the basis for the segregation of spatial and nonspatial cues at higher cortical levels. Some units exhibited significant nonlinear interactions between particular combinations of pitch, timbre, and azimuth. These interactions were most pronounced for pitch and timbre and were less commonly observed between spatial and nonspatial attributes. Such nonlinearities were most prevalent in primary auditory cortex, although they tended to be small compared with stimulus main effects.

Cortico‐cortical connectivity within ferret auditory cortex

“…Because the physiologically identified areas differ in their sensitivity to spatial and nonspatial features of a sound source (Bizley and King, 2008; Bizley et al, 2009; Bizley et al, 2010), an open question is the extent to which they represent different processing pathways, and how these areas relate to cortical fields in other species. To address these questions, a series of retrograde and anterograde injections (Table 1) were made in a total of 13 ferrets to examine the projections within and between each of the physiologically or anatomically defined auditory areas.…”

“…Previous tracer studies in ferret revealed that these areas are innervated by the ventral division of the MGB (Pallas et al, 1990), and that multiple areas, predominantly on the PEG, but also on the AEG, receive connections from the MEG (Wallace and Bajwa, 1991; Pallas and Sur, 1993; Gao and Pallas, 1999). Since these studies were completed, we have gained a deeper understanding of the functional organization of the auditory cortex as assessed by responses to both simple (Kowalski et al, 1995; Nelken et al, 2004; Bizley et al, 2005, 2007a) and complex stimuli (Nelken et al, 2008; Bizley et al, 2009, 2013; Atiani et al, 2014), warranting a more comprehensive investigation of the connectivity within the auditory cortex. Our anatomical investigations support the idea that distinct anterior and posterior processing pathways exist and extend our understanding about the organization of the auditory cortex in the ferret, thus providing crucial information to facilitate cross‐species comparisons.…”

“…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). …”

Large-Scale Heterogeneous Representation of Sound Attributes in Rat Primary Auditory Cortex: From Unit Activity to Population Dynamics

“…While studying the topological characteristics of the neuronal response in A1 to auditory stimuli, researchers subsequently insert electrodes in different cortical locations, e.g., tungsten microelectrodes (Doron et al, 2002;Rutkowski et al, 2003) and silicon-based laminar (Sakata and Harris, 2009) and planar (Lakatos et al, 2007;Bizley et al, 2009Bizley et al, , 2010 probes. This strategy has two major drawbacks: (1) the tissue condition deteriorates with each insertion and (2) it is hard to evaluate the actual probe location because of successive contractions/expansions of a small cortical area that may occasionally induce tissue swelling and bleeding.…”

“…Still, it needs to be clarified whether the same or different neuronal assemblies take part in codifying sound time envelopes through a spatial segregation strategy. Some studies have reported a pitch-selective area near the low-frequency border of A1 [monkeys Wang, 2005, 2010), ferrets (Bizley et al, 2009(Bizley et al, , 2010], whereas others claim peculiar spatial organizations [e.g., Mongolian gerbils, circular gradient (Schulze et al, 2002); cats, linear gradient (Langner et al, 2009)]. Neurons sensitive to the modulation frequency are uniformly distributed in A1 [rats (Kilgard and Merzenich, 1999), monkeys Wang, 2005, 2010)].…”