Processing of location and pattern changes of natural sounds in the human auditory cortex

Parallel cortical pathways have been proposed for the processing of auditory pattern and spatial information, respectively. We tested this segregation with human functional magnetic resonance imaging (fMRI) and separate electroencephalographic (EEG) recordings in the same subjects who listened passively to four sequences of repetitive spatial animal vocalizations in an event-related paradigm. Transitions between sequences constituted either a change of auditory pattern, location, or both pattern+location. This procedure allowed us to investigate the cortical correlates of natural auditory "what" and "where" changes independent of differences in the individual stimuli. For pattern changes, we observed significantly increased fMRI responses along the bilateral anterior superior temporal gyrus and superior temporal sulcus, the planum polare, lateral Heschl's gyrus and anterior planum temporale. For location changes, significant increases of fMRI responses were observed in bilateral posterior superior temporal gyrus and planum temporale. An overlap of these two types of changes occurred in the lateral anterior planum temporale and posterior superior temporal gyrus. The analysis of source event-related potentials (ERPs) revealed faster processing of location than pattern changes. Thus, our data suggest that passive processing of auditory spatial and pattern changes is dissociated both temporally and anatomically in the human brain. The predominant role of more anterior aspects of the superior temporal lobe in sound identity processing supports the role of this area as part of the auditory pattern processing stream, while spatial processing of auditory stimuli appears to be mediated by the more posterior parts of the superior temporal lobe.     

Left thalamo-cortical network implicated in successful speech separation and identification

The separation of concurrent sounds is paramount to human communication in everyday settings. The primary auditory cortex and the planum temporale are thought to be essential for both the separation of physical sound sources into perceptual objects and the comparison of those representations with previously learned acoustic events. To examine the role of these areas in speech separation, we measured brain activity using event-related functional Magnetic Resonance Imaging (fMRI) while participants were asked to identify two phonetically different vowels presented simultaneously. The processing of brief speech sounds (200 ms in duration) activated the thalamus and superior temporal gyrus bilaterally, left anterior temporal lobe, and left inferior temporal gyrus. A comparison of fMRI signals between trials in which participants successfully identified both vowels as opposed to when only one of the two vowels was recognized revealed enhanced activity in left thalamus, Heschl's gyrus, superior temporal gyrus, and the planum temporale. Because participants successfully identified at least one of the two vowels on each trial, the difference in fMRI signal indexes the extra computational work needed to segregate and identify successfully the other concurrently presented vowel. The results support the view that auditory cortex in or near Heschl's gyrus as well as in the planum temporale are involved in sound segregation and reveal a link between left thalamo-cortical activation and the successful separation and identification of simultaneous speech sounds.     

Abnormal association between reduced magnetic mismatch field to speech sounds and smaller left planum temporale volume in schizophrenia

Schizophrenia is associated with language-related dysfunction. A previous study [Schizophr. Res. 59 (2003c) 159] has shown that this abnormality is present at the level of automatic discrimination of change in speech sounds, as revealed by magnetoencephalographic recording of auditory mismatch field in response to across-category change in vowels. Here, we investigated the neuroanatomical substrate for this physiological abnormality. Thirteen patients with schizophrenia and 19 matched control subjects were examined using magnetoencephalography (MEG) and high-resolution magnetic resonance imaging (MRI) to evaluate both mismatch field strengths in response to change between vowel /a/ and /o/, and gray matter volumes of Heschl's gyrus (HG) and planum temporale (PT). The magnetic global field power of mismatch response to change in phonemes showed a bilateral reduction in patients with schizophrenia. The gray matter volume of left planum temporale, but not right planum temporale or bilateral Heschl's gyrus, was significantly smaller in patients with schizophrenia compared with that in control subjects. Furthermore, the phonetic mismatch strength in the left hemisphere was significantly correlated with left planum temporale gray matter volume in patients with schizophrenia only. These results suggest that structural abnormalities of the planum temporale may underlie the functional abnormalities of fundamental language-related processing in schizophrenia.     

Effective connectivity analysis demonstrates involvement of premotor cortex during speech perception

Several reports of premotor cortex involvement in speech perception have been put forward. Still, the functional role of premotor cortex is under debate. In order to investigate the functional role of premotor cortex, we presented parametrically varied speech stimuli in both a behavioral and functional magnetic resonance imaging (fMRI) study. White noise was transformed over seven distinct steps into a speech sound and presented to the participants in a randomized order. As control condition served the same transformation from white noise into a music instrument sound. The fMRI data were modelled with Dynamic Causal Modeling (DCM) where the effective connectivity between Heschl's gyrus, planum temporale, superior temporal sulcus and premotor cortex were tested. The fMRI results revealed a graded increase in activation in the left superior temporal sulcus. Premotor cortex activity was only present at an intermediate step when the speech sounds became identifiable but were still distorted but was not present when the speech sounds were clearly perceivable. A Bayesian model selection procedure favored a model that contained significant interconnections between Heschl's gyrus, planum temporal, and superior temporal sulcus when processing speech sounds. In addition, bidirectional connections between premotor cortex and superior temporal sulcus and from planum temporale to premotor cortex were significant. Processing non-speech sounds initiated no significant connections to premotor cortex. Since the highest level of motor activity was observed only when processing identifiable sounds with incomplete phonological information, it is concluded that premotor cortex is not generally necessary for speech perception but may facilitate interpreting a sound as speech when the acoustic input is sparse.     

Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains

We used voxel-based morphometry (VBM) to examine human brain asymmetry and the effects of sex and handedness on brain structure in 465 normal adults. We observed significant asymmetry of cerebral grey and white matter in the occipital, frontal, and temporal lobes (petalia), including Heschl's gyrus, planum temporale (PT) and the hippocampal formation. Males demonstrated increased leftward asymmetry within Heschl's gyrus and PT compared to females. There was no significant interaction between asymmetry and handedness and no main effect of handedness. There was a significant main effect of sex on brain morphology, even after accounting for the larger global volumes of grey and white matter in males. Females had increased grey matter volume adjacent to the depths of both central sulci and the left superior temporal sulcus, in right Heschl's gyrus and PT, in right inferior frontal and frontomarginal gyri and in the cingulate gyrus. Females had significantly increased grey matter concentration extensively and relatively symmetrically in the cortical mantle, parahippocampal gyri, and in the banks of the cingulate and calcarine sulci. Males had increased grey matter volume bilaterally in the mesial temporal lobes, entorhinal and perirhinal cortex, and in the anterior lobes of the cerebellum, but no regions of increased grey matter concentration.     

Neuromagnetic representation of musical register information in human auditory cortex

Pulse-resonance sounds like vowels or instrumental tones contain acoustic information about the physical size of the sound source (pulse rate) and body resonators (resonance scale). Previous research has revealed correlates of these variables in humans using functional neuroimaging. Here, we report two experiments that use magnetoencephalography to study the neuromagnetic representations of pulse rate and resonance scale in human auditory cortex. In Experiment 1, auditory evoked fields were recorded from nineteen subjects presented with French horn tones, the pulse rate and resonance scale of which had been manipulated independently using a mucoder. In Experiment 2, fifteen subjects listened to French horn tones which differed in resonance scale but which lacked pulse rate cues. The resulting cortical activity was evaluated by spatio-temporal source analysis. Changes in pulse rate elicited a well-defined N1m component with cortical generators located at the border between Heschl's gyrus and planum temporale. Changes in resonance scale elicited a second, independent, N1m component located in planum temporale. Our results demonstrate that resonance scale can be distinguished in its neuromagnetic representation from cortical activity related to the sound's pulse rate. Moreover, the existence of two separate components in the N1m sensitive to register information highlights the importance of this time window for the processing of frequency information in human auditory cortex.     

Scanning silence: mental imagery of complex sounds

In this functional magnetic resonance imaging (fMRI) study, we investigated the neural basis of mental auditory imagery of familiar complex sounds that did not contain language or music. In the first condition (perception), the subjects watched familiar scenes and listened to the corresponding sounds that were presented simultaneously. In the second condition (imagery), the same scenes were presented silently and the subjects had to mentally imagine the appropriate sounds. During the third condition (control), the participants watched a scrambled version of the scenes without sound. To overcome the disadvantages of the stray acoustic scanner noise in auditory fMRI experiments, we applied sparse temporal sampling technique with five functional clusters that were acquired at the end of each movie presentation. Compared to the control condition, we found bilateral activations in the primary and secondary auditory cortices (including Heschl's gyrus and planum temporale) during perception of complex sounds. In contrast, the imagery condition elicited bilateral hemodynamic responses only in the secondary auditory cortex (including the planum temporale). No significant activity was observed in the primary auditory cortex. The results show that imagery and perception of complex sounds that do not contain language or music rely on overlapping neural correlates of the secondary but not primary auditory cortex.     

The morphometry of auditory cortex in the congenitally deaf measured using MRI

The study of congenitally deaf individuals provides a unique opportunity to understand the organization and potential for reorganization of human auditory cortex. We used magnetic resonance imaging (MRI) to examine the structural organization of two auditory cortical regions, Heschl's gyrus (HG) and the planum temporale (PT), in deaf and hearing subjects. The results show preservation of cortical volume in HG and PT of deaf subjects deprived of auditory input since birth. Measurements of grey and white matter, as well as the location and extent of these regions in the deaf showed complete overlap both with matched controls and with previous samples of hearing subjects. The results of the manual volume measures were supported by findings from voxel-based morphometry analyses that showed increased grey-matter density in the left motor hand area of the deaf, but no differences between the groups in any auditory cortical region. This increased cortical density in motor cortex may be related to more active use of the dominant hand in signed languages. Most importantly, expected interhemispheric asymmetries in HG and PT thought to be related to auditory language processing were preserved in these deaf subjects. These findings suggest a strong genetic component in the development and maintenance of auditory cortical asymmetries that does not depend on auditory language experience. Preservation of cortical volume in the deaf suggests plasticity in the input and output of auditory cortex that could include language-specific or more general-purpose information from other sensory modalities.     

Representation of lateralization and tonotopy in primary versus secondary human auditory cortex

Functional MRI was performed to investigate differences in the basic functional organization of the primary and secondary auditory cortex regarding preferred stimulus lateralization and frequency. A modified sparse acquisition scheme was used to spatially map the characteristics of the auditory cortex at the level of individual voxels. In the regions of Heschl's gyrus and sulcus that correspond with the primary auditory cortex, activation was systematically strongest in response to contralateral stimulation. Contrarily, in the surrounding secondary active regions including the planum polare and the planum temporale, large-scale preferences with respect to stimulus lateralization were absent. Regarding optimal stimulus frequency, low- to high-frequency spatial gradients were discernable along the Heschl's gyrus and sulcus in anterolateral to posteromedial direction, especially in the right hemisphere, consistent with the presence of a tonotopic organization in these primary areas. However, in the surrounding activated secondary areas frequency preferences were erratic. Lateralization preferences did not depend on stimulus frequency, and frequency preferences did not depend on stimulus lateralization. While the primary auditory cortex is topographically organized with respect to physical stimulus properties (i.e., lateralization and frequency), such organizational principles are no longer obvious in secondary and higher areas. This suggests a neural re-encoding of sound signals in the transition from primary to secondary areas, possibly in relation to auditory scene analysis and the processing of auditory objects.     

Brain activation mediates the association between structural abnormality and symptom severity in schizophrenia

Thought disorder is a symptom of schizophrenia expressed as disorganized or incoherent speech. Severity of thought disorder correlates with decreased left superior temporal gyrus grey matter volume and cortical activation in posterior temporal regions during the performance of language tasks. The goal of this study was to determine whether language-related activation mediates the association between thought disorder and left superior temporal lobe grey matter volume. 12 patients with schizophrenia were assessed for thought disorder. FMRI images were acquired for each subject while they listened to English speech, along with a high resolution structural image. Thought disorder was used as a covariate in the functional analysis to identify brain regions within which activation correlated with symptom severity. Voxel based morphometry was used to calculate grey matter volume of the planum temporale. A mediation model waste-tested using a four-step multiple regression approach incorporating cortical volume, functional activation and symptom severity. Thought disorder correlated with activation in a single cluster within the left posterior middle temporal gyrus during listening to speech. Grey matter volume within the planum temporale correlated significantly with severity of thought disorder and activation within the functional cluster. Regressing thought disorder on grey matter volume and BOLD response simultaneously led to a significant reduction in the correlation between grey matter volume and thought disorder. These results support the hypothesis that the association between decreased grey matter volume in the left planum temporale and severity of thought disorder is mediated by activation in the posterior temporal lobe during language processing.     

Listening to a walking human activates the temporal biological motion area

A vivid perception of a moving human can be evoked when viewing a few point-lights on the joints of an invisible walker. This special visual ability for biological motion perception has been found to involve the posterior superior temporal sulcus (STSp). However, in everyday life, human motion can also be recognized using acoustic cues. In the present study, we investigated the neural substrate of human motion perception when listening to footsteps, by means of a sparse sampling functional MRI design. We first showed an auditory attentional network that shares frontal and parietal areas previously found in visual attention paradigms. Second, an activation was observed in the auditory cortex (Heschl's gyrus and planum temporale), likely to be related to low-level sound processing. Most strikingly, another activation was evidenced in a STSp region overlapping the temporal biological motion area previously reported using visual input. We thus propose that a part of the STSp region might be a supramodal area involved in human motion recognition, irrespective of the sensory modality input.     

Functional fields in human auditory cortex revealed by time-resolved fMRI without interference of EPI noise

The gradient switching during fast echoplanar functional magnetic resonance imaging (EPI-fMRI) produces loud noises that may interact with the functional activation of the central auditory system induced by experimental acoustic stimuli. This interaction is unpredictable and is likely to confound the interpretation of functional maps of the auditory cortex. In the present study we used an experimental design which does not require the presentation of stimuli during EPI acquisitions and allows for mapping of the auditory cortex without the interference of scanner noise. The design relies on the physiological delays between the onset, or the end, of stimulation and the corresponding hemodynamic response. Owing to these delays and through a time-resolved acquisition protocol it is possible to analyze the decay of the stimulus-specific signal changes after the cessation of the stimulus itself and before the onset of the EPI-acoustic noise related activation (decay-sampling technique). This experimental design, which might permit a more detailed insight in the auditory cortex, has been applied to the study of the cortical responses to pulsed 1000 Hz sine tones. Distinct activation clusters were detected in the Heschl's gyri and the planum temporale, with an increased extension compared to a conventional block-design paradigm. Furthermore, the comparison of the hemodynamic response of the most anterior and the posterior clusters of activation highlighted differential response patterns to the sound stimulation and to the EPI-noise. These differences, attributable to reciprocal saturation effects unevenly distributed over the superior temporal cortex, provided evidence for functionally distinct auditory fields.     

Manual and automated measures of superior temporal gyrus asymmetry: concordant structural predictors of verbal ability in children

The planum temporale is a region on the posterior surface of the temporal lobe that exhibits robust leftward structural asymmetry, which has been linked to verbal ability in children and adults. Traditionally, structural asymmetry has been quantified with manual assessment of high resolution MRI scans. Such measures require subjective and frequently unreliable determination of highly variable anatomical boundaries. Methodological developments in automated image processing (voxel-based morphometry - VBM) offer the opportunity to obtain objective and reliable measures of structural variation. This study examined the extent to which a VBM measure of gray matter asymmetry in the posterior superior temporal gyrus (pSTG) characterized the same individual variation as a manual measure of planum temporale asymmetry in 99 healthy adults and 39 typically developing children. Planum temporale asymmetry was significantly correlated with pSTG gray matter asymmetry in the samples of adults and children. As a measure of validity we examined the extent to which the VBM measure of pSTG gray matter asymmetry predicted measures of verbal ability that were associated with the manual measure of planum temporale asymmetry in the same children. The two asymmetry measures predicted the same variance in verbal ability. The automated measure of pSTG gray matter asymmetry predicted additional significant variance in verbal ability, however. In addition, a posterior STS region was also identified that significantly predicted verbal ability. These results demonstrate significant advantages of an automated voxel-based measure over a manual measure of planum temporale asymmetry.     

Positional and surface area asymmetry of the human cerebral cortex

Previous studies of cortical asymmetry have relied mainly on voxel-based morphometry (VBM), or manual segmentation of regions of interest. This study uses fully automated, surface-based techniques to analyse position and surface area asymmetry for the mid-surfaces of 112 right-handed subjects' cortical hemispheres from a cohort of young adults. Native space measurements of local surface area asymmetry and vertex position asymmetry were calculated from surfaces registered to a previously validated hemisphere-unbiased surface-based template. Our analysis confirms previously identified hemispheric asymmetries (Yakovlevian torque, frontal and occipital petalia) in enhanced detail. It does not support previous findings of gender/asymmetry interactions or rightward planum parietale areal increase. It reveals several new findings, including a striking leftward increase in surface area of the supramarginal gyrus (peak effect 18%), compared with a smaller areal increase in the left Heschl's gyrus and planum temporale region (peak effect 8%). A second finding was rightward increase in surface area (peak effect 10%) in a band around the medial junction between the occipital lobe, and parietal and temporal lobes. By clearly separating out the effects of structural translocation and surface area change from those of thickness and curvature, this study resolves the confound of these variables inherent in VBM studies.     

Response preferences for "what" and "where" in human non-primary auditory cortex

Primate studies suggest the auditory cortex is organized in at least two anatomically and functionally separate pathways: a ventral pathway specializing in object recognition and a dorsal pathway specializing in object localization. The current experiment assesses the validity of this model in human listeners using fMRI to investigate the neural substrates of spatial and non-spatial temporal pattern information. Targets were differentiated from non-targets on the basis of two levels of pitch information (present vs. absent, fixed vs. varying) and two levels of spatial information (compact vs. diffuse sound source, fixed vs. varying location) in a factorial design. Analyses revealed spatially separate responses to spatial and non-spatial temporal information. The main activation associated with pitch occurred predominantly in Heschl's gyrus (HG) and planum polare, while that associated with changing sound source location occurred posterior to HG, in planum temporale (PT). Activation common to both pitch and changing spatial location was located bilaterally in anterior PT. Apart from this small region of overlap, our data support the anatomical and functional segregation of 'what' and 'where' in human non-primary auditory cortex. Our results also highlight a distinction in the sensitivity of anterior and posterior fields of PT to non-spatial information and specify the type of spatial information that is coded within early areas of the spatial processing stream.     

Bach speaks: a cortical "language-network" serves the processing of music

The aim of the present study was the investigation of neural correlates of music processing with fMRI. Chord sequences were presented to the participants, infrequently containing unexpected musical events. These events activated the areas of Broca and Wernicke, the superior temporal sulcus, Heschl's gyrus, both planum polare and planum temporale, as well as the anterior superior insular cortices. Some of these brain structures have previously been shown to be involved in music processing, but the cortical network comprising all these structures has up to now been thought to be domain-specific for language processing. To what extent this network might also be activated by the processing of non-linguistic information has remained unknown. The present fMRI-data reveal that the human brain employs this neuronal network also for the processing of musical information, suggesting that the cortical network known to support language processing is less domain-specific than previously believed.     

BOLD correlates of edge detection in human auditory cortex

Edges are important cues defining coherent auditory objects. As a model of auditory edges, sound on- and offset are particularly suitable to study their neural underpinnings because they contrast a specific physical input against no physical input. Change from silence to sound, that is onset, has extensively been studied and elicits transient neural responses bilaterally in auditory cortex. However, neural activity associated with sound onset is not only related to edge detection but also to novel afferent inputs. Edges at the change from sound to silence, that is offset, are not confounded by novel physical input and thus allow to examine neural activity associated with sound edges per se. In the first experiment, we used silent acquisition functional magnetic resonance imaging and found that the offset of pulsed sound activates planum temporale, superior temporal sulcus and planum polare of the right hemisphere. In the planum temporale and the superior temporal sulcus, offset response amplitudes were related to the pulse repetition rate of the preceding stimulation. In the second experiment, we found that these offset-responsive regions were also activated by single sound pulses, onset of sound pulse sequences and single sound pulse omissions within sound pulse sequences. However, they were not active during sustained sound presentation. Thus, our data show that circumscribed areas in right temporal cortex are specifically involved in identifying auditory edges. This operation is crucial for translating acoustic signal time series into coherent auditory objects.     

Volumetric vs. surface-based alignment for localization of auditory cortex activation

The high degree of intersubject structural variability in the human brain is an obstacle in combining data across subjects in functional neuroimaging experiments. A common method for aligning individual data is normalization into standard 3D stereotaxic space. Since the inherent geometry of the cortex is that of a 2D sheet, higher precision can potentially be achieved if the intersubject alignment is based on landmarks in this 2D space. To examine the potential advantage of surface-based alignment for localization of auditory cortex activation, and to obtain high-resolution maps of areas activated by speech sounds, fMRI data were analyzed from the left hemisphere of subjects tested with phoneme and tone discrimination tasks. We compared Talairach stereotaxic normalization with two surface-based methods: Landmark Based Warping, in which landmarks in the auditory cortex were chosen manually, and Automated Spherical Warping, in which hemispheres were aligned automatically based on spherical representations of individual and average brains. Examination of group maps generated with these alignment methods revealed superiority of the surface-based alignment in providing precise localization of functional foci and in avoiding mis-registration due to intersubject anatomical variability. Human left hemisphere cortical areas engaged in complex auditory perception appear to lie on the superior temporal gyrus, the dorsal bank of the superior temporal sulcus, and the lateral third of Heschl's gyrus.     

Cytochrome Oxidase, Acetylcholinesterase, and NADPH-Diaphorase Staining in Human Supratemporal and Insular Cortex: Evidence for Multiple Auditory Areas

The pattern of cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase activity was studied in the supratemporal plane, the posterior part of the superior temporal gyrus, and the insula of normal human brains. Five dark cytochrome oxidase regions were found: (i) on Heschl's gyrus (area TC of von Economo and Koskinas); (ii) on the planum polare (area TC/TG); (iii) posterior to Heschl's gyrus (within area TA); (iv) on the posterior convexity of the superior temporal gyrus (within area TA); and (v) on the posterosuperior insula (area IB). More lightly stained cortex separated these regions (areas IA, TD, and part of TB). The laminar distribution of cytochrome oxidase activity varied in different areas. Acetylcholinesterase-positive fibers predominated in area TC and pyramidal neurons in areas TA and IA and in parts of TB; a mixture of fiber and neuronal staining was found in TC/TG, TD, and IB. NADPH-diaphorase positive profiles included large darkly stained nonpyramidal neurons, mostly in infragranular layers and in subcortical white matter, small faintly stained cells, and a dense array of fibers. The NADPH-diaphorase staining pattern did not vary between areas. The present results suggest that the supratemporal plane, the posterior part of the superior temporal gyrus, and the insula contain at least eight putative cortical areas. Comparison with activation studies by others suggest that, apart from the primary auditory area, six other putative areas may be auditory whereas one putative area, on posterior insula, may be vestibular.     

Diffeomorphic metric surface mapping in subregion of the superior temporal gyrus

This paper describes the application of large deformation diffeomorphic metric mapping to cortical surfaces based on the shape and geometric properties of subregions of the superior temporal gyrus in the human brain. The anatomical surfaces of the cortex are represented as triangulated meshes. The diffeomorphic matching algorithm is implemented by defining a norm between the triangulated meshes, based on the algorithms of Vaillant and Glaunès. The diffeomorphic correspondence is defined as a flow of the extrinsic three dimensional coordinates containing the cortical surface that registers the initial and target geometry by minimizing the norm. The methods are demonstrated in 40 high-resolution MRI cortical surfaces of planum temporale (PT) constructed from subsets of the superior temporal gyrus (STG). The effectiveness of the algorithm is demonstrated via the Euclidean positional distance, distance of normal vectors, and curvature before and after the surface matching as well as the comparison with a landmark matching algorithm. The results demonstrate that both the positional and shape variability of the anatomical configurations are being represented by the diffeomorphic maps.