Neuroplasticity of semantic representations for musical instruments in professional musicians

Professional musicians constitute a model par excellence for understanding experience-dependent plasticity in the human brain, particularly in the auditory domain. Their intensive sensorimotor experience with musical instruments has been shown to entail plastic brain alterations in cortical perceptual and motor maps. It remains an important question whether this neuroplasticity might extend beyond basic perceptual and motor functions and even shape higher-level conceptualizations by which we conceive our physical and social world. Here we show using functional magnetic resonance imaging (fMRI) that conceptual processing of visually presented musical instruments activates auditory association cortex encompassing right posterior superior temporal gyrus, as well as adjacent areas in the superior temporal sulcus and the upper part of middle temporal gyrus (pSTG/MTG) only in musicians, but not in musical laypersons. These areas in and adjacent to auditory association cortex were not only recruited by conceptual processing of musical instruments during visual object recognition, but also by auditory perception of real sounds. Hence, the unique intensive experience of musicians with musical instruments establishes a link between auditory perceptual and conceptual brain systems. Experience-driven neuroplasticity in musicians is thus not confined to alterations of perceptual and motor maps, but even leads to the establishment of higher-level semantic representations for musical instruments in and adjacent to auditory association cortex. These findings highlight the eminent importance of sensory and motor experience for acquiring rich concepts.     

Neural mechanisms underlying auditory feedback control of speech

The neural substrates underlying auditory feedback control of speech were investigated using a combination of functional magnetic resonance imaging (fMRI) and computational modeling. Neural responses were measured while subjects spoke monosyllabic words under two conditions: (i) normal auditory feedback of their speech and (ii) auditory feedback in which the first formant frequency of their speech was unexpectedly shifted in real time. Acoustic measurements showed compensation to the shift within approximately 136 ms of onset. Neuroimaging revealed increased activity in bilateral superior temporal cortex during shifted feedback, indicative of neurons coding mismatches between expected and actual auditory signals, as well as right prefrontal and Rolandic cortical activity. Structural equation modeling revealed increased influence of bilateral auditory cortical areas on right frontal areas during shifted speech, indicating that projections from auditory error cells in posterior superior temporal cortex to motor correction cells in right frontal cortex mediate auditory feedback control of speech.     

Differential brain activation patterns during perception of voice and tone onset time series: a MEG study

Evoked magnetic fields were recorded from 18 adult volunteers using magnetoencephalography (MEG) during perception of speech stimuli (the endpoints of a voice onset time (VOT) series ranging from /ga/ to /ka/), analogous nonspeech stimuli (the endpoints of a two-tone series varying in relative tone onset time (TOT), and a set of harmonically complex tones varying in pitch. During the early time window (approximately 60 to approximately 130 ms post-stimulus onset), activation of the primary auditory cortex was bilaterally equal in strength for all three tasks. During the middle (approximately 130 to 800 ms) and late (800 to 1400 ms) time windows of the VOT task, activation of the posterior portion of the superior temporal gyrus (STGp) was greater in the left hemisphere than in the right hemisphere, in both group and individual data. These asymmetries were not evident in response to the nonspeech stimuli. Hemispheric asymmetries in a measure of neurophysiological activity in STGp, which includes the supratemporal plane and cortex inside the superior temporal sulcus, may reflect a specialization of association auditory cortex in the left hemisphere for processing speech sounds. Differences in late activation patterns potentially reflect the operation of a postperceptual process (e.g., rehearsal in working memory) that is restricted to speech stimuli.     

The musician's brain: functional imaging of amateurs and professionals during performance and imagery

We compared activation maps of professional and amateur violinists during actual and imagined performance of Mozart's violin concerto in G major (KV216). Execution and imagination of (left hand) fingering movements of the first 16 bars of the concerto were performed. Electromyography (EMG) feedback was used during imagery training to avoid actual movement execution and EMG recording was employed during the scanning of both executed and imagined musical performances. We observed that professional musicians generated higher EMG amplitudes during movement execution and showed focused cerebral activations in the contralateral primary sensorimotor cortex, the bilateral superior parietal lobes, and the ipsilateral anterior cerebellar hemisphere. The finding that professionals exhibited higher activity of the right primary auditory cortex during execution may reflect an increased strength of audio-motor associative connectivity. It appears that during execution of musical sequences in professionals, a higher economy of motor areas frees resources for increased connectivity between the finger sequences and auditory as well as somatosensory loops, which may account for the superior musical performance. Professionals also demonstrated more focused activation patterns during imagined musical performance. However, the auditory-motor loop was not involved during imagined performances in either musician group. It seems that the motor and auditory systems are coactivated as a consequence of musical training but only if one system (motor or auditory) becomes activated by actual movement execution or live musical auditory stimuli.     

Effective connectivity during haptic perception: a study using Granger causality analysis of functional magnetic resonance imaging data

Although it is accepted that visual cortical areas are recruited during touch, it remains uncertain whether this depends on top-down inputs mediating visual imagery or engagement of modality-independent representations by bottom-up somatosensory inputs. Here we addressed this by examining effective connectivity in humans during haptic perception of shape and texture with the right hand. Multivariate Granger causality analysis of functional magnetic resonance imaging (fMRI) data was conducted on a network of regions that were shape- or texture-selective. A novel network reduction procedure was employed to eliminate connections that did not contribute significantly to overall connectivity. Effective connectivity during haptic perception was found to involve a variety of interactions between areas generally regarded as somatosensory, multisensory, visual and motor, emphasizing flexible cooperation between different brain regions rather than rigid functional separation. The left postcentral sulcus (PCS), left precentral gyrus and right posterior insula were important sources of connections in the network. Bottom-up somatosensory inputs from the left PCS and right posterior insula fed into visual cortical areas, both the shape-selective right lateral occipital complex (LOC) and the texture-selective right medial occipital cortex (probable V2). In addition, top-down inputs from left postero-supero-medial parietal cortex influenced the right LOC. Thus, there is strong evidence for the bottom-up somatosensory inputs predicted by models of visual cortical areas as multisensory processors and suggestive evidence for top-down parietal (but not prefrontal) inputs that could mediate visual imagery. This is consistent with modality-independent representations accessible through both bottom-up sensory inputs and top-down processes such as visual imagery.     

Early multisensory interactions affect the competition among multiple visual objects

In dynamic cluttered environments, audition and vision may benefit from each other in determining what deserves further attention and what does not. We investigated the underlying neural mechanisms responsible for attentional guidance by audiovisual stimuli in such an environment. Event-related potentials (ERPs) were measured during visual search through dynamic displays consisting of line elements that randomly changed orientation. Search accuracy improved when a target orientation change was synchronized with an auditory signal as compared to when the auditory signal was absent or synchronized with a distractor orientation change. The ERP data show that behavioral benefits were related to an early multisensory interaction over left parieto-occipital cortex (50-60 ms post-stimulus onset), which was followed by an early positive modulation (80-100 ms) over occipital and temporal areas contralateral to the audiovisual event, an enhanced N2pc (210-250 ms), and a contralateral negative slow wave (CNSW). The early multisensory interaction was correlated with behavioral search benefits, indicating that participants with a strong multisensory interaction benefited the most from the synchronized auditory signal. We suggest that an auditory signal enhances the neural response to a synchronized visual event, which increases the chances of selection in a multiple object environment.     

Neural changes associated with speech learning in deaf children following cochlear implantation

Brain plasticity was investigated, which underlies the gaining of auditory sensory and/or auditory language in deaf children with an early onset deafness after cochlear implantation (CI) surgery. This study examined both the glucose metabolism of the brain and the auditory speech learning using 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) and the Central Institute of Deaf (CID) test, respectively, both before and after the CI surgery. In a within analysis comparing the pre-CI and the post-CI PET results, CI itself resulted in an increase in the glucose metabolism in the medial visual cortex, the bilateral thalamus, and the posterior cingulate. Compared with the normal hearing controls, the brain activity of the deaf children was greater in the medial visual cortex and bilateral occipito-parietal junctions after the CI. The better speech perception ability was associated with increases in activity in the higher visual areas such as middle occipito-temporal junction (hMT/V5) and posterior inferior temporal region (BA 21/37) in the left hemisphere and associated with decreases in activity in the right inferior parieto-dorsal prefrontal region. These findings suggest that the speech learning resulted in a greater demand of the visual and visuospatial processings subserved by the early visual cortex and parietal cortices. However, only those deaf children who successfully learned the auditory language after CI used more visual motion perception for mouth movement in the left hMT/V5 region and less somatosensory function in the right parieto-frontal region.     

Gamma-band activity over early sensory areas predicts detection of changes in audiovisual speech stimuli

Oscillatory activity in the gamma-band range in human magneto- and electroencephalogram is thought to reflect the oscillatory synchronization of cortical networks. Findings of enhanced gamma-band activity (GBA) during cognitive processes like gestalt perception, attention and memory have led to the notion that GBA may reflect the activation of internal object representations. However, there is little direct evidence suggesting that GBA is related to subjective perceptual experience. In the present study, magnetoencephalogram was recorded during an audiovisual oddball paradigm with infrequent visual (auditory /ta/ + visual /pa/) or acoustic deviants (auditory /pa/ + visual /ta/) interspersed in a sequence of frequent audiovisual standard stimuli (auditory /ta/ + visual /ta/). Sixteen human subjects had to respond to perceived acoustic changes which could be produced either by real acoustic or illusory (visual) deviants. Statistical probability mapping served to identify correlations between oscillatory activity in response to visual and acoustic deviants, respectively, and the detection rates for either type of deviant. The perception of illusory acoustic changes induced by visual deviants was closely associated with gamma-band amplitude at approximately 80 Hz between 250 and 350 ms over midline occipital cortex. In contrast, the detection of real acoustic deviants correlated positively with induced GBA at approximately 42 Hz between 200 and 300 ms over left superior temporal cortex and negatively with evoked gamma responses at approximately 41 Hz between 220 and 240 ms over occipital areas. These findings support the relevance of high-frequency oscillatory activity over early sensory areas for perceptual experience.     

Modality effects in verbal working memory: differential prefrontal and parietal responses to auditory and visual stimuli

The neural bases of verbal (nonspatial) working memory (VWM) have been primarily examined using visual stimuli. Few studies have investigated the neural bases of VWM using auditory stimuli, and fewer have explored modality differences in VWM. In this study, we used functional magnetic resonance imaging (fMRI) to examine similarities and differences between visual VWM (vis-VWM) and auditory VWM (aud-VWM) utilizing identical stimuli and a within-subjects design. Performance levels were similar in the two modalities and there was extensive overlap of activation bilaterally in the dorsolateral and ventrolateral prefrontal cortex (DLPFC and VLPFC), intraparietal sulcus, supramarginal gyrus and the basal ganglia. However, a direct statistical comparison revealed significant modality differences: the left posterior parietal cortex, primarily along the intraparietal sulcus, showed greater responses during vis-VWM whereas the left dorsolateral prefrontal cortex showed greater responses during aud-VWM. No such differences were observed in the right hemisphere. Other modality differences in VWM were also observed, but they were associated with relative decreases in activation. In particular, we detected bilateral suppression of the superior and middle temporal (auditory) cortex during vis-VWM, and of the occipital (visual) cortex during aud-VWM, thus suggesting that cross-modal inhibitory processes may help to provide preferential access to high-order heteromodal association areas. Taken together, our findings suggest that although similar prefrontal and parietal regions are involved in aud-VWM and vis-VWM, there are important modality differences in the way neural signals are generated, processed and routed during VWM.     

Right rolandic activation during speech perception in stutterers: a MEG study

The focus of our magnetoencephalographic (MEG) study was to obtain further insight into the neuronal organization of language processing in stutterers. We recorded neuronal activity of 10 male developmental stutterers and 10 male controls, while they listened to pure tones, to words in order to repeat them, and to sentences in order to either repeat or transform them into passive form. Stimulation with pure tones resulted in similar activation patterns in the two groups, but differences emerged in the more complex auditory language tasks. In the stutterers, the left inferior frontal cortex was activated for a short while from 95 to 145 ms after sentence onset, which was not evident in the controls nor in either group during the word task. In both subject groups, the left rolandic area was activated when listening to the speech stimuli, but in the stutterers, there was an additional activation of the right rolandic area from 315 ms onwards, which was more pronounced in the sentence than word task. Activation of areas typically associated with language production was thus observed also during speech perception both in controls and in stutterers. Previous research on speech production in stutterers has found abnormalities in both the amount and timing of activation in these areas. The present data suggest that activation in the left inferior frontal and right rolandic areas in stutterers differs from that in controls also during speech perception.     

The dorsal auditory pathway is involved in performance of both visual and auditory rhythms

We used functional magnetic resonance imaging to investigate the effect of two factors on the neural control of temporal sequence performance: the modality in which the rhythms had been trained, and the modality of the pacing stimuli preceding performance. The rhythms were trained 1-2 days before scanning. Each participant learned two rhythms: one was presented visually, the other auditorily. During fMRI, the rhythms were performed in blocks. In each block, four beats of a visual or auditory pacing metronome were followed by repetitive self-paced rhythm performance from memory. Data from the self-paced performance phase was analysed in a 2x2 factorial design, with the two factors Training Modality (auditory or visual) and Metronome Modality (auditory or visual), as well as with a conjunction analysis across all active conditions, to identify activations that were independent of both Training Modality and Metronome Modality. We found a significant main effect only for visual versus auditory Metronome Modality, in the left angular gyrus, due to a deactivation of this region after auditory pacing. The conjunction analysis revealed a set of brain areas that included dorsal auditory pathway areas (left temporo-parietal junction area and ventral premotor cortex), dorsal premotor cortex, the supplementary and presupplementary premotor areas, the cerebellum and the basal ganglia. We conclude that these regions are involved in controlling performance of well-learned rhythms, regardless of the modality in which the rhythms are trained and paced. This suggests that after extensive short-term training, all rhythms, even those that were both trained and paced in visual modality, had been transformed into auditory-motor representations. The deactivation of the angular cortex following auditory pacing may represent cross-modal auditory-visual inhibition.     

Evidence for a frontal cortex role in both auditory and somatosensory habituation: a MEG study

Auditory and somatosensory responses to paired stimuli were investigated for commonality of frontal activation that may be associated with gating using magnetoencephalography (MEG). A paired stimulus paradigm for each sensory evoked study tested right and left hemispheres independently in ten normal controls. MR-FOCUSS, a current density technique, imaged simultaneously active cortical sources. Each subject showed source localization, in the primary auditory or somatosensory cortex, for the respective stimuli following both the first (S1) and second (S2) impulses. Gating ratios for the auditory M50 response, equivalent to the P50 in EEG, were 0.54+/-0.24 and 0.63+/-0.52 for the right and left hemispheres. Somatosensory gating ratios were evaluated for early and late latencies as the pulse duration elicits extended response. Early gating ratios for right and left hemispheres were 0.69+/-0.21 and 0.69+/-0.41 while late ratios were 0.81+/-0.41 and 0.80+/-0.48. Regions of activation in the frontal cortex, beyond the primary auditory or somatosensory cortex, were mapped within 25 ms of peak S1 latencies in 9/10 subjects during auditory stimulus and in 10/10 subjects for somatosensory stimulus. Similar frontal activations were mapped within 25 ms of peak S2 latencies for 75% of auditory responses and for 100% of somatosensory responses. Comparison between modalities showed similar frontal region activations for 17/20 S1 responses and for 13/20 S2 responses. MEG offers a technique for evaluating cross modality gating. The results suggest similar frontal sources are simultaneously active during auditory and somatosensory habituation.     

Single-trial EEG-fMRI coupling of the emotional auditory early posterior negativity

Event-related potential (ERP) studies in the visual domain often report an emotion-evoked early posterior negativity (EPN). Studies in the auditory domain have recently shown a similar component. Little source localization has been done on the visual EPN, and no source localization has been done on the auditory EPN. The aim of the current study was to identify the neural generators of the auditory EPN using EEG-fMRI single-trial coupling. Data were recorded from 19 subjects who completed three auditory choice reaction tasks: (1) a control task using neutral tones; (2) a prosodic emotion task involving the categorization of syllables; and (3) a semantic emotion task involving the categorization of words. The waveforms of the emotion tasks diverged from the neutral task over parietal scalp during a very early time window (132-156 ms) and later during a more traditional EPN time window (252-392 ms). In the EEG-fMRI analyses, the variance of the voltage in the earlier time window was correlated with activity in the medial prefrontal cortex, but only in the word task. In the EEG-fMRI analyses of the traditional EPN time window both emotional tasks covaried with activity in the left superior parietal lobule. Our results support previous parietal cortex source localization findings for the visual EPN, and suggest enhanced selective attention to emotional stimuli during the EPN time window.     

Different distribution of the activated areas in the dorsal premotor cortex during visual and auditory reaction-time tasks.

Sensorimotor association is an essential aspect of behavior. The dorsal part of the premotor cortex (PMd) is known to have an important role in sensorimotor association. Although it is suggested that the partially segregated groups of neurons are involved in sensorimotor association in different sensory modalities, it is not yet clear whether these groups occupy the PMd to the same or different extent. Therefore, we performed a functional magnetic resonance imaging study to compare activated regions in the PMd during simple reaction-time tasks with visual and auditory cues. Eight normal volunteers performed two simple reaction time tasks with a conventional on-off design; one is with a visual cue and the other is with an auditory cue. In both tasks, two regions in the left primary motor area (M1) (4a and 4p) and the bilateral PMd were activated. The two activated regions in the left M1 occupied the same areas in both the visual and the auditory tasks. However, in the PMd, the activated regions were situate medially during the visual task and laterally during the auditory task, along the precentral sulci. There was no overlap of significantly activated regions between two tasks, and areas specifically activated during the visual task were observed in the middle of the precentral sulci, bilaterally. The results suggest that the distribution of PMd subregions involved in sensorimotor association differ when the sensory cues are in different modalities.     

Exploring the contributions of premotor and parietal cortex to spatial compatibility using image-guided TMS

Functional brain imaging studies have demonstrated increased activity in dorsal premotor and posterior parietal cortex when performing spatial stimulus-response compatibility tasks (SRC). We tested the specific role of these regions in stimulus-response mapping using single-pulse transcranial magnetic stimulation (TMS). Subjects were scanned using functional magnetic resonance imaging (fMRI) prior to the TMS session during performance of a task in which spatial compatibility was manipulated. For each subject, the area of increased signal within the regions of interest was registered onto their own high-resolution T1-weighted anatomic scan. TMS was applied to these areas for each subject using a frameless stereotaxic system. Task accuracy and reaction time (RT) were measured during blocks of compatible or incompatible trials and during blocks of real TMS or sham stimulation. On each trial, a single TMS pulse was delivered at 50, 100, 150, or 200 ms after the onset of the stimulus in the left or right visual field. TMS over the left premotor cortex produced various facilitatory effects, depending on the timing of the stimulation. At short intervals, TMS appeared to prime the left dorsal premotor cortex to select a right-hand response more quickly, regardless of stimulus-response compatibility. The strongest effect of stimulation, however, occurred at the 200-ms interval, when TMS facilitated left-hand responses during the incompatible condition. Facilitation of attention to the contralateral visual hemifield was observed during stimulation over the parietal locations. We conclude that the left premotor cortex is one of the cortical regions responsible for overriding automatic stimulus-response associations.     

Activation of the human posterior parietal and temporoparietal cortices during audiotactile interaction

We recorded cortical-evoked responses with a whole-scalp neuromagnetometer to study human brain dynamics associated with audiotactile interaction. The subjects received unilateral auditory (A) or tactile (T) stimuli, or both stimuli simultaneously (AT), alternating to the left and right side. Responses to AT stimuli differed significantly from the algebraic sum of responses to A and T stimuli (A + T) at 75-85 and 105-130 ms and indicated suppressive audiotactile interaction. Source modeling revealed that the earlier interaction occurred in the contralateral posterior parietal cortex and the later interaction in the contralateral parietal opercula between the SII cortex and the auditory cortex. The interaction was significantly stronger in the left than the right hemisphere. In most subjects, AT responses were far more similar to T than to A responses, suggesting suppression of auditory processing during the spatially and temporally concordant audiotactile stimuli in which the tactile component was subjectively more salient.     

The involvement of ipsilateral temporoparietal cortex in tactile pattern working memory as reflected in beta event-related desynchronization

Cortical oscillatory activity in various frequency bands has been shown to reflect working memory processes operating on visual and auditory stimulus information. Here we use magnetoencephalography to investigate cortical oscillatory activity related to working memory for tactile patterns. Right-handed subjects made same-different judgements on two dot patterns sequentially applied with a 3-s delay to the right middle fingertip. Spectral analysis revealed beta desynchronization (17+/-2.5 Hz) at contralateral postcentral and ipsilateral temporoparietal regions preceding and during the presentation of both tactile stimuli as well as during the early and late delay periods. Whereas contralateral beta desynchronization preceding tactile stimulation may reflect anticipation of incoming stimuli, ipsilateral beta desynchronization may underlie working memory maintenance of tactile patterns. The later hypothesis is supported by a significant positive correlation between subjects' performance and the amplitude of ipsilateral beta desynchronization 800 ms to 500 ms before the onset of the second pattern stimulus. Thus, our results suggest that ipsilateral temporoparietal cortex contributes to the maintenance of tactile pattern information in working memory.     

Frontal and temporal dysfunction of auditory stimulus processing in schizophrenia

Attention deficits have been consistently described in schizophrenia. Functional neuroimaging and electrophysiological studies have focused on anterior cingulate cortex (ACC) dysfunction as a possible mediator. However, recent basic research has suggested that the effect of attention is also observed as a relative amplification of activity in modality-associated cortical areas. In the present study, the question was addressed whether an amplification deficit is seen in the auditory cortex of schizophrenic patients during an attention-requiring choice reaction task. Twenty-one drug-free schizophrenic patients and 21 age- and sex-matched healthy controls were studied (32-channel EEG). The underlying generators of the event-related N1 component were separated in neuroanatomic space using a minimum-norm (LORETA) and a multiple dipole (BESA) approach. Both methods revealed activation in the primary auditory cortex (peak latency approximately 100 ms) and in the area of the ACC (peak latency approximately 130 ms). In addition, the adapted multiple dipole model also showed a temporal-radial source activation in nonprimary auditory areas (peak latency approximately 140 ms). In schizophrenic patients, significant activation deficits were found in the ACC as well as in the left nonprimary auditory areas that differentially correlated with negative and positive symptoms. The results suggest that (1) the source in the nonprimary auditory cortex is detected only with a multiple dipole approach and (2) that the N1 generators in the ACC and in the nonprimary auditory cortex are dysfunctional in schizophrenia. This would be in line with the notion that attention deficits in schizophrenia involve an extended cortical network.     

Multisensory speech perception without the left superior temporal sulcus

Converging evidence suggests that the left superior temporal sulcus (STS) is a critical site for multisensory integration of auditory and visual information during speech perception. We report a patient, SJ, who suffered a stroke that damaged the left tempo-parietal area, resulting in mild anomic aphasia. Structural MRI showed complete destruction of the left middle and posterior STS, as well as damage to adjacent areas in the temporal and parietal lobes. Surprisingly, SJ demonstrated preserved multisensory integration measured with two independent tests. First, she perceived the McGurk effect, an illusion that requires integration of auditory and visual speech. Second, her perception of morphed audiovisual speech with ambiguous auditory or visual information was significantly influenced by the opposing modality. To understand the neural basis for this preserved multisensory integration, blood-oxygen level dependent functional magnetic resonance imaging (BOLD fMRI) was used to examine brain responses to audiovisual speech in SJ and 23 healthy age-matched controls. In controls, bilateral STS activity was observed. In SJ, no activity was observed in the damaged left STS but in the right STS, more cortex was active in SJ than in any of the normal controls. Further, the amplitude of the BOLD response in right STS response to McGurk stimuli was significantly greater in SJ than in controls. The simplest explanation of these results is a reorganization of SJ's cortical language networks such that the right STS now subserves multisensory integration of speech.