Elsevier

Cortex

Volume 49, Issue 10, November–December 2013, Pages 2822-2833
Cortex

Research report
Spatial representations of temporal and spectral sound cues in human auditory cortex

https://doi.org/10.1016/j.cortex.2013.04.003Get rights and content

Abstract

Natural and behaviorally relevant sounds are characterized by temporal modulations of their waveforms, which carry important cues for sound segmentation and communication. Still, there is little consensus as to how this temporal information is represented in auditory cortex. Here, by using functional magnetic resonance imaging (fMRI) optimized for studying the auditory system, we report the existence of a topographically ordered spatial representation of temporal sound modulation rates in human auditory cortex. We found a topographically organized sensitivity within auditory cortex to sounds with varying modulation rates, with enhanced responses to lower modulation rates (2 and 4 Hz) on lateral parts of Heschl's gyrus (HG) and faster modulation rates (16 and 32 Hz) on medial HG. The representation of temporal modulation rates was distinct from the representation of sound frequencies (tonotopy) that was orientated roughly orthogonal. Moreover, the combination of probabilistic anatomical maps with a previously proposed functional delineation of auditory fields revealed that the distinct maps of temporal and spectral sound features both prevail within two presumed primary auditory fields hA1 and hR. Our results reveal a topographically ordered representation of temporal sound cues in human primary auditory cortex that is complementary to maps of spectral cues. They thereby enhance our understanding of the functional parcellation and organization of auditory cortical processing.

Introduction

Natural and behaviorally relevant sounds are often characterized by prominent amplitude modulations of their temporal envelope. Amplitude modulation in speech, for example, provides linguistic information and modulation rates up to 50 Hz often serve as cues to segment speech tokens (Giraud and Poeppel, 2012; Luo and Poeppel, 2007; Rosen, 1992). Slow envelope modulations are not only critical for speech understanding (Elliott and Theunissen, 2009) but speech recognition solely based on slow temporal envelope cues is surprising good (Drullman et al., 1994; Shannon et al., 1995). In music, individual notes (complex periodic sounds played by an instrument) occur mostly at rates of a few Hertz, while faster modulation rates (>40 Hz) characterize the pitch of individual instrumental sounds (Plack et al., 2005). Importantly, regular temporal envelope modulations are not confined to human communication signals, but are a characteristic feature of animal vocalizations and many other natural sounds (Chandrasekaran et al., 2009; Joris et al., 2004). In general, slow modulation rates of a few Hertz are perceived as individual events, with rates of a few tens of Hertz producing a gradually more blended percept known as acoustic flutter (Bendor and Wang, 2007; Miller and Taylor, 1948). Even faster modulation rates above approximately 40 Hz result in a continuous percept that is usually associated with a specific perceived pitch (Pressnitzer et al., 2001) and contribute to distinguishing speaker identities, emotional states or different environmental sounds (Latinus and Belin, 2011; Rosen, 1992; Singh and Theunissen, 2003). Despite the importance of these slow temporal envelope modulations in natural sounds for carrying behaviorally relevant information, it remains unresolved how auditory cortex represents these. Here, we emphasize on the cortical representation of sound envelope modulation in a range between 2 and 32 Hz that is crucial for communication but which does not induce a specific pitch percept.

In many auditory structures spectral sound features are represented as spatial (tonotopic) maps, whereby the neural organization of preferred sound frequency reflects the ordered frequency representation in the cochlea (Formisano et al., 2003; Petkov et al., 2006). These topographically ordered functional maps of spectral cues are observed consistently across species, and are used for the functional parcellation of auditory cortices into individual fields (Formisano et al., 2003; Merzenich and Brugge, 1973; Merzenich et al., 1975; Petkov et al., 2006; Recanzone et al., 2000). In general, maps representing features from the sensory environment are a common organizational principle across auditory, visual and sensory cortices (Formisano et al., 2003; Knudsen et al., 1987; Penfield and Boldrey, 1937; Sereno et al., 1995; Yu et al., 2005). These maps feature systematic spatial distributions of sensory information within a cortical area, providing computational advantages in sensory information processing (Knudsen et al., 1987). For the auditory system, various maps featuring different behaviorally relevant aspects of sound analysis have been observed [for review see Schreiner and Winer (2007)]. Given the behavioral importance of temporal sound cues several authors have argued for a similar spatially ordered representation of temporal modulation rates in auditory cortex (Moore, 2003; Schreiner and Winer, 2007). Indeed, animal studies have provided evidence for spatial encoding of temporal envelope cues in the auditory midbrain of the monkey (Baumann et al., 2011). However, other studies found no evidence for a consistent spatial representation of temporal sound cues in auditory cortex (Bendor and Wang, 2010; Nelken et al., 2008).

Despite clear evidence for selectivity to temporal sound features in individual neurons (Bendor and Wang, 2007, 2010; Imaizumi et al., 2011), it remains unclear whether in humans (i) auditory cortices provide spatially distinct representations of this neural selectivity of temporal sound cues, and (ii) how this presumed spatial representation of temporal sound features relates to auditory fields as defined either by anatomy or tonotopic maps. Here we combined an functional magnetic resonance imaging (fMRI) sequence optimized for imaging the auditory system (Seifritz et al., 2006) with a stimulation protocol commonly used to reveal topographical cortical sensory representations (Engel et al., 1994) to test for topographically ordered representations of temporal envelope modulation in human auditory cortex, and to compare these maps with those representing spectral sound features (i.e., tonotopic maps) within the same subjects.

Section snippets

Subjects

The experiments were approved by the joint ethics committee of the University Clinic and the Max Planck Institute, Tübingen, Germany, and all subjects provided written informed consent to participate in this study. Six adult subjects (three males, three females, ages 23–36; five right- and one left-handed) participated in the study. No subject had a history of neurological or hearing disorders. During data acquisition subjects were asked to keep eyes open and to listen to the sounds.

Data acquisition

fMRI data

Spatial representation of sound frequency

We first determined the representation of sound frequency to identify the tonotopic organization of auditory cortices within our subjects (Exp. 1). We presented sweeps of pulsed sine-wave tones with stepwise increasing spectral frequency (500–8000 Hz; Exp. 1, Figs. 1 and 2) and identified sites preferentially and significantly (FDR p < .01) activated by particular frequencies using a cortex-based alignment technique projected relative to the cytoarchitectonic organization around Heschl's gyrus

The representation of temporal sound cues in auditory cortex

Our results demonstrate a distinct spatial representation of temporal sound modulation rates in human PAC that was consistently revealed across subjects and hemispheres. This representation of temporal sound cues exhibits a topographical organization alongside HG that is orthogonal to the representation of spectral sound frequency (tonotopy). This finding propels speculations as to the use of a place coding or place preference for temporal sound features in auditory cortex, a hypothesis that is

Acknowledgments

This work was supported by the Swiss National Science Foundation and the ‘Schweizerische Stiftung für medizinisch-biologische Stipendien’ (Grant PASMP3-123222, M.H.) and the Max Planck Society.

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