Representation of lateralization and tonotopy in primary versus secondary human auditory cortex
Introduction
The central auditory system is organized into hierarchically organized processing stages that are distributed over several structures in the brainstem, midbrain, thalamus, and cerebral cortex. Numerous studies have been carried out in humans and primates regarding the parcellation and functional organization of the auditory cortex in particular. As a result, a distinction has been made between primary processing areas that form a core region in the superior surface of the temporal lobe, and secondary areas that are located in an adjacent belt region. In addition, associative and multimodal regions in a parabelt area and various other areas are thought to be involved in higher order processing of auditory information (Kaas et al., 1999).
The distinction between primary and secondary auditory processing areas has originally been made on the basis of differences in cytoarchitectonic features, i.e., the cell densities, types, and sizes in the various cortical layers (Brodmann, 1909, Morosan et al., 2001, Rademacher et al., 2001, Shapleske et al., 1999). However, functional differences have been reported as well. For instance, some studies have reported that responses occur slightly earlier in primary auditory cortex than in secondary cortex (Belin et al., 1999, Liegeois-Chauvel et al., 1994). Whereas both primary and secondary regions respond during the perception of sound, only secondary regions are active during sound imagery (Bunzeck et al., 2005). Furthermore, the primary auditory cortex has been found to respond to a broad range of auditory stimuli, while the secondary cortex seems to respond preferably to stimuli with sufficiently complex spectral dynamics (Specht and Reul, 2003, Thivard et al., 2000). Secondary regions have been reported to be sensitive to slower temporal modulations and broader spectral modulations than primary regions, indicating that some form of temporal and spectral integration is taking place (Giraud et al., 2000, Langers et al., 2003). This may indicate a specialization towards the processing of acoustic and phonetic sound features in primary and secondary auditory regions, respectively, which may be corroborated by the role of the planum temporale in the analysis of voice onset times (Jäncke et al., 2002a). Still, we note that the role of secondary auditory regions in spectro-temporal processing is likely broader than for speech alone (Griffiths and Warren, 2002).
Two basic features regarding the functional organization of the auditory cortex that have been well established in animal studies and that have also been confirmed in humans (Konig et al., 2005) are [i] the contralateral dominance of responses to monaural stimulation and [ii] the presence of tonotopic gradients on the cortical surface. However, neuroimaging studies in humans that concern these characteristics mostly report summary values for the auditory cortices as a whole. For instance, response lateralization is usually quantified using a laterality index that expresses the lateralization of the extent or magnitude of activation (Bilecen et al., 2000, Jäncke et al., 2002b, Scheffler et al., 1998, Woldorff et al., 1999). Tonotopic progressions have often been demonstrated by mapping effective activation foci in response to a range of stimulus frequencies, e.g., using source locations in electro/magnetoencephalography (Cansino et al., 2003, Fujioka et al., 2003, Langner et al., 1997, Liegeois-Chauvel et al., 2001, Romani et al., 1982) and observations or calculations of the ‘center of mass’ of activation clusters in positron emission tomography and functional magnetic resonance imaging (fMRI) (Bilecen et al., 1998, Engelien et al., 2002, Lockwood et al., 1999, Schmid et al., 1998, Schönwiesner et al., 2002, Wessinger et al., 1997, Yetkin et al., 2004). Such methods quantify overall response behavior but do not distinguish between functional subdivisions of the auditory cortex. Therefore, they will not reveal differences in the functional characteristics between, e.g., the primary and secondary auditory cortices. To our knowledge, small-scale spatial variations in preferences regarding stimulus lateralization have not yet been mapped, and although some recent studies thoroughly characterized the cortical gradients in optimal stimulus frequency (Formisano et al., 2003, Talavage et al., 2004), tonotopic arrangements in humans are not fully understood either.
The aim of this study was to reinvestigate response lateralization and tonotopic organization by mapping both the optimal stimulus lateralization and frequency at the detailed level of individual voxels. An active listening task and an adapted fMRI paradigm were employed to improve the detection of activation signals. Furthermore, by investigating both response lateralization and tonotopic organization in a single study, the presence of interactions between these two characteristics could be assessed for the first time.
Section snippets
Subjects
Ten healthy subjects were recruited on the basis of written informed consent, in approved accordance with the requirements of the medical ethical committee at the Maastricht University Hospital. The subjects comprised 3 females (#1–#3) and 7 males (#4–#10); 7 subjects were right-handed (#1–#7), 2 left-handed (#8–#9), and 1 ambidextrous (#10) (Oldfield, 1971). Ages ranged from 23 to 43 years (mean 31 years). All subjects were tested by an audiologist using standard pure tone audiometry (Katz,
Activation characteristics
The activation in the auditory cortex in response to the various stimuli was determined using T-test statistics. Fig. 2 shows the activation patterns that were found for individual subjects as well as for the group as a whole. To facilitate the comparison of activation patterns and mappings between subjects, differences in the overall level of activation were taken into account by adjusting the statistical thresholds in such a way that equal volumes of activation were detected for each subject.
Discussion
In this study, cortical activation was determined in response to monaurally and binaurally presented stimuli of various frequencies. The response characteristics of individual voxels were calculated and compared to the whole brain average to determine their relative preferences regarding stimulus lateralization and frequency. Results were visualized to show the presence of topographic mappings in various subdivisions of the auditory cortices. The significance of differences in lateralization
Conclusion
In summary, we found that at the first stages of cortical auditory processing both hemispheres respond most strongly to the contralateral ear. Also, we provided further evidence for a tonotopic organization in the primary auditory cortices. In contrast, at higher processing levels in the auditory cortex (i.e., in secondary and higher cortical auditory areas) no systematic preferences with regard to stimulus lateralization and frequency were obvious. Our findings support the hypothesis that the
Acknowledgments
This work was supported by the Research Fund of the University Hospital Maastricht and the Heinsius Houbolt Foundation. Furthermore, the authors would like to acknowledge the contribution of L. Speelman, who participated in the development of some of the initial data processing routines.
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