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.     

Magnetoencephalographic correlates of audiotactile interaction

To seek for correlates of an interaction between auditory and somatosensory processing, the brain's magnetic field in response to simultaneously presented auditory (A) and tactile (T) stimuli was compared with the sum of the respective unimodal responses (A+T). The stimuli were binaural 1047-Hz tone bursts of 60 dB sensation level and tactile pressure pulses to the right thumb. The mean interval between two stimuli of the same modality was 1.95 s. The magnetic field was recorded using a 306-channel whole-scalp neuromagnetometer. A clear audiotactile interaction was revealed in the hemisphere contralateral to the side of tactile stimulation in six of eight subjects, whereas in the ipsilateral hemisphere an interaction was noticed in only three subjects. The time courses of these audiotactile interaction fields typically showed major deflections of opposite polarities around 140 and 220 ms. The first deflection appeared to arise in the region of the secondary somatosensory cortex (SII). The polarity of this interaction was consistent with the view that the auditory stimulus resulted in a partial inhibition in SII. In two subjects, strong indications of auditory contributions to the interaction were available, although in different hemispheres. The relatively high interindividual variability of the observed interaction, which represents potential neural substrates for multisensory integration, could indicate that the way subjects perceive the simultaneous presentation of auditory and tactile stimuli differs.     

Towards natural stimulation in fMRI--issues of data analysis

In search for suitable tools to study brain activation in natural environments, where the stimuli are multimodal, poorly predictable and irregularly varying, we collected functional magnetic resonance imaging data from 6 subjects during a continuous 8-min stimulus sequence that comprised auditory (speech or tone pips), visual (video clips dominated by faces, hands, or buildings), and tactile finger stimuli in blocks of 6-33 s. Results obtained by independent component analysis (ICA) and general-linear-model-based analysis (GLM) were compared. ICA separated in the superior temporal gyrus one independent component (IC) that reacted to all auditory stimuli and in the superior temporal sulcus another IC responding only to speech. Several distinct and rather symmetric vision-sensitive ICs were found in the posterior brain. An IC in the V5/MT region reacted to videos depicting faces or hands, whereas ICs in the V1/V2 region reacted to all video clips, including buildings. The corresponding GLM-derived activations in the auditory and early visual cortices comprised sub-areas of the ICA-revealed activations. ICA separated a prominent IC in the primary somatosensory cortex whereas the GLM-based analysis failed to show any touch-related activation. "Intrinsic" components, unrelated to the stimuli but spatially consistent across subjects, were discerned as well. The individual time courses were highly consistent in sensory projection cortices and more variable elsewhere. The ability to differentiate functionally meaningful composites of activated brain areas and to straightforwardly reveal their temporal dynamics renders ICA a sensitive tool to study brain responses to complex natural stimuli.     

Touch, sound and vision in human superior temporal sulcus

Human superior temporal sulcus (STS) is thought to be a key brain area for multisensory integration. Many neuroimaging studies have reported integration of auditory and visual information in STS but less is known about the role of STS in integrating other sensory modalities. In macaque STS, the superior temporal polysensory area (STP) responds to somatosensory, auditory and visual stimulation. To determine if human STS contains a similar area, we measured brain responses to somatosensory, auditory and visual stimuli using blood-oxygen level dependent functional magnetic resonance imaging (BOLD fMRI). An area in human posterior STS, STSms (multisensory), responded to stimulation in all three modalities. STSms responded during both active and passive presentation of unisensory somatosensory stimuli and showed larger responses for more intense vs. less intense tactile stimuli, hand vs. foot, and contralateral vs. ipsilateral tactile stimulation. STSms showed responses of similar magnitude for unisensory tactile and auditory stimulation, with an enhanced response to simultaneous auditory-tactile stimulation. We conclude that STSms is important for integrating information from the somatosensory as well as the auditory and visual modalities, and could be the human homolog of macaque STP.     

The left fusiform gyrus hosts trisensory representations of manipulable objects

During object manipulation the brain integrates the visual, auditory, and haptic experience of an object into a unified percept. Previous brain imaging studies have implicated for instance the dorsal part of the lateral occipital complex in visuo-tactile and the posterior superior temporal sulcus in audio-visual integration of object-related inputs (Amedi et al., 2005). Yet it is still unclear which brain regions represent object-specific information of all three sensory modalities. To address this question, we performed two complementary functional magnetic resonance imaging experiments. In the first experiment, we identified brain regions which were consistently activated by unimodal visual, auditory, and haptic processing of manipulable objects relative to non-object control stimuli presented in the same modality. In the second experiment, we assessed regional brain activations when participants had to match object-related information that was presented simultaneously in two or all three modalities. Only a well-defined region in left fusiform gyrus (FG) showed an object-specific activation during unisensory processing in the visual, auditory, and tactile modalities. The same region was also consistently activated during multisensory matching of object-related information across all three senses. Taken together, our results suggest that this region is central to the recognition of manipulable objects. A putative role of this FG region is to unify object-specific information provided by the visual, auditory, and tactile modalities into trisensory object representations.     

Differential fMRI activation to noxious heat and tactile stimuli in parasylvian areas of new world monkeys

Emerging evidence supports an important role of posterior parasylvian areas in both pain and touch processing. Whether there are separate or shared networks for these sensations remains controversial. The present study compared spatial patterns of brain activation in response to unilateral nociceptive heat (47.5°C) or innocuous tactile stimulation (8-Hz vibration) to digits through high-resolution functional magnetic resonance imaging (fMRI) in squirrel monkeys. In addition, the temporal profile of heat-stimulus-evoked fMRI Blood Oxygenation Level Dependent (BOLD) signal changes was characterized. By examining high-resolution fMRI and histological measures at both the individual and the group levels, we found that both nociceptive heat and tactile stimuli elicited activation in bilateral secondary somatosensory and ventral parietal areas (S2/PV) and in ipsilateral ventral somatosensory areas (VS) and retroinsula (Ri). Bilateral posterior insular cortex (pIns) and area 7b responded preferentially to nociceptive heat stimulation. Single voxels within each activation cluster showed robust BOLD signal changes during each block of nociceptive stimulation. Across animals (n = 11), nociceptive response magnitudes of contralateral VS and pIns and ipsilateral Ri were significantly greater than corresponding areas in the opposite hemisphere. In sum, both distinct and shared areas in regions surrounding the posterior sylvian fissure were activated in response to nociceptive and tactile inputs in nonhuman primates.     

Neural correlates of counting of sequential sensory and motor events in the human brain

Little is known about the ability to enumerate small numbers of successive stimuli and movements. It is possible that there exist neural substrates that are consistently recruited both to count sensory stimuli from different modalities and for counting movements executed by different effectors. Here, we identify a network of areas that was involved in enumerating small numbers of auditory, visual, and somatosensory stimuli, and in enumerating sequential movements of hands and feet, in the bilateral premotor cortex, presupplementary motor area, posterior temporal cortex, and thalamus. The most significant consistent activation across sensory and motor counting conditions was found in the lateral premotor cortex. Lateral premotor activation was not dependent on movement preparation, stimulus presentation timing, or number word verbalization. Movement counting, but not sensory counting, activated the anterior parietal cortex. This anterior parietal area may correspond to an area recruited for movement counting identified by recent single-neuron studies in monkeys. These results suggest that overlapping but not identical networks of areas are involved in counting sequences of sensory stimuli and sequences of movements in the human brain.     

The neural basis of temporal auditory discrimination

When two identical stimuli, such as a pair of clicks, are presented with a sufficiently long time-interval between them they are readily perceived as two separate events. However, as they are presented progressively closer together, there comes a point when the two separate stimuli are perceived as one. This phenomenon applies not only to hearing but also to other sensory modalities. Damage to the basal ganglia disturbs this type of temporal discrimination irrespective of sensory modality, suggesting a multimodal process is involved. Our aim was to study the neural substrate of auditory temporal discrimination in healthy subjects and to compare it with structures previously associated with analogous tactile temporal discrimination. During fMRI scanning, paired-clicks separated by variable inter-stimulus intervals (1-50 ms) were delivered binaurally, with different intensities delivered to each ear, yielding a lateralised auditory percept. Subjects were required (a) to report whether they heard one or two stimuli (TD: temporal discrimination); or (b) to report whether the stimuli were located on the right or left side of the head mid-line (SD: spatial discrimination); or (c) simply to detect the presence of an auditory stimulus (control task). Our results showed that both types of auditory discrimination (TD and SD) compared to simple detection activated a network of brain areas including regions of prefrontal cortex and basal ganglia. Critically, two clusters in pre-SMA and the anterior cingulate cortex were specifically activated by TD. Furthermore, these clusters overlap with regions activated for similar judgments in the tactile modality suggesting that they fulfill a multimodal function in the temporal processing of sensory events.     

Critical period for cross-modal plasticity in blind humans: a functional MRI study

The primary visual cortex (V1) in congenitally blind humans has been shown to be involved in tactile discrimination tasks, indicating that there is a shift in function of this area of cortex, but the age dependency of the reorganization is not fully known. To investigate the reorganized network, we measured the change of regional cerebral blood flow using 3.0 Tesla functional MRI during passive tactile tasks performed by 15 blind and 8 sighted subjects. There was increased activity in the postcentral gyrus to posterior parietal cortex and decreased activity in the secondary somatosensory area in blind compared with sighted subjects during a tactile discrimination task. This suggests that there is a greater demand for shape discrimination processing in blind subjects. Blind subjects, irrespective of the age at onset of blindness, exhibited higher activity in the visual association cortex than did sighted subjects. V1 was activated in blind subjects who lost their sight before 16 years of age, whereas it was suppressed in blind subjects who lost their sight after 16 years of age during a tactile discrimination task. This suggests that the first 16 years of life represent a critical period for a functional shift of V1 from processing visual stimuli to processing tactile stimuli. Because of the age-dependency, V1 is unlikely to be the "entry node" of the cortex for the redirection of tactile signals into visual cortices after blinding. Instead, the visual association cortex may mediate the circuitry by which V1 is activated during tactile stimulation.     

Spatial resolution of fMRI in the human parasylvian cortex: comparison of somatosensory and auditory activation

In spite of its outstanding spatial resolution, the biological resolution of functional MRI may be worse because it depends on the vascular architecture of the brain. Here, we compared the activation patterns of the secondary somatosensory and parietal ventral cortex (SII/PV) with that of the primary auditory cortex and adjacent areas (AI/AII). These two brain regions are located immediately adjacent to each other on opposite banks of the Sylvian fissure, and are anatomically and functionally distinct. In 12 healthy subjects, SII/PV was activated by pneumatic tactile stimuli applied to the index finger (0.5 cm2 contact area, 4 bar pressure), and AI/AII by amplitude-modulated tones (800 Hz carrier frequency, modulated at 24-36 Hz). Functional images were obtained with a 1.5-T scanner and were evaluated using SPM99. Sensitivity of fMRI activation in this unselected sample was 71% for tactile and 83% for auditory stimulation. Group analysis showed activation of SII/PV by tactile and activation of three locations in AI/AII by auditory stimuli. Distributions extended to the opposite side of the fissure (19-58% after tactile and 13-14% after auditory stimulation, depending on the side of stimulation/hemisphere). Morphometry of individual sulcal anatomy revealed that the course of the Sylvian fissure varied by 5.3 mm (SD) in vertical direction. Taking this into account, SII/PV was located 5.8 +/- 2.7 mm above the Sylvian fissure, whereas AI/AII was located 6.3 +/- 1.7 mm below the Sylvian fissure. Even in individual analysis, the most significant voxel after tactile stimuli in one subject was found on the "wrong" side of the fissure; this error could be ascribed to the spatial normalization procedure. These data show that fMRI signals may overlap substantially, even if the activated regions are separated by 12 mm across a major sulcus. Spatial normalization to an atlas template can introduce additional variance. Individual sulcal anatomy should be preferred over mean atlas locations.     

Functional MR imaging: paradigms for clinical preoperative mapping

Clinical applications of functional MR imaging include mapping of brain functions in relationship to intracranial tumors, seizure foci, or vascular malformations to determine the risk for performing surgical excision, the need for intraoperative mapping during excision, and selecting the optimal surgical approach to a lesion. A variety of paradigms are used to produce a blood-oxygen-level-dependent response in various brain regions, which can be identified with functional MR imaging. The paradigms used include active motor, language, or cognitive tasks, and passive tactile, auditory, or visual stimuli. Activation usually indicates the location of eloquent cortex. Lack of function in a region cannot be assumed when functional MR imaging shows absence of activation within the region.     

Temporo-spatial analysis of cortical activation by phasic innocuous and noxious cold stimuli--a magnetoencephalographic study

Clinical findings and recent non-invasive functional imaging studies pinpoint the insular cortex as the crucial brain area involved in cold sensation. By contrast, the role of primary (SI) and secondary (SII) somatosensory cortices in central processing of cold is controversial. So far, temporal activation patterns of cortical areas involved in cold processing have not been examined. Using magnetoencephalography, we studied, in seven healthy subjects, the temporo-spatial dynamics of brain processes evoked by innocuous and noxious cold stimulation as compared to tactile stimuli. For this purpose, a newly designed and magnetically silent cold-stimulator was employed. In separate runs, cold and painful cold stimuli were delivered to the dorsum of the right hand. Tactile afferents were stimulated by pneumatic tactile stimulation.

Following innocuous cold stimulation (ΔT=5±0.3°C in 50±2 ms), magnetic source imaging revealed an exclusive activation of the contra- and ipsilateral posterior insular cortex. The mean peak latencies were 194.3±38.1 and 241.0±31.7 ms for the response in the ipsi- and contralateral insular cortex, respectively. Based on the measurement of onset latencies, the estimated conduction velocity of peripheral nerve fibres mediating cold fell in the range of Aδ-fibres (7.4±0.8 m/s).

Noxious cold stimulation (ΔT=35±5°C in 70±12 ms) initially activated the contra- and ipsilateral insular cortices in the same latency ranges as innocuous cold stimuli. Additionally, we found an activation of the contra- and ipsilateral SII areas (peak latencies 304±22.7 and 310.1±19.4 ms, respectively) and a variable activation of the cingulate cortex. Notably, neither cold- nor painful cold stimulation produced an activation of SI. By contrast, the evoked cortical responses following tactile stimulation could be located to the contralateral SI cortex and bilateral SII.

In conclusion, this study strongly corroborates the posterior insular cortex as the primary somatosensory area for cortical processing of cold sensation. Furthermore, it supports the role of SII and the cingulate cortex in mediating freeze-pain. Therefore, these results suggest different processing of cold, freeze-pain and touch in the human brain.     

Differential patterns of multisensory interactions in core and belt areas of human auditory cortex

The auditory cortex is anatomically segregated into a central core and a peripheral belt region, which exhibit differences in preference to bandpassed noise and in temporal patterns of response to acoustic stimuli. While it has been shown that visual stimuli can modify response magnitude in auditory cortex, little is known about differential patterns of multisensory interactions in core and belt. Here, we used functional magnetic resonance imaging and examined the influence of a short visual stimulus presented prior to acoustic stimulation on the spatial pattern of blood oxygen level-dependent signal response in auditory cortex. Consistent with crossmodal inhibition, the light produced a suppression of signal response in a cortical region corresponding to the core. In the surrounding areas corresponding to the belt regions, however, we found an inverse modulation with an increasing signal in centrifugal direction. Our data suggest that crossmodal effects are differentially modulated according to the hierarchical core-belt organization of auditory cortex.     

Thermal and tactile sensory deficits and allodynia in a nerve-injured patient: a multimodal psychophysical and functional magnetic resonance imaging study

OBJECTIVE: A case study was conducted to examine a patient with chronic neuropathic pain of the right foot following peripheral nerve injury and characterize associated sensory abnormalities. METHODS: Multimodal psychophysical examination of the patient's affected and nonaffected foot included thermal sensibility, dynamic touch, and directional sensibility. In addition, we used functional magnetic resonance imaging to study cortical representation of brush-evoked allodynia. RESULTS: Detailed psychophysical examination revealed substantial deficits in warm, cool, and tactile perception on the injured foot. These findings indicated severe dysfunction of perceptual processes mediated by A beta, A delta, and C fibers. Despite reduced tactile perception, light touch evoked a deep burning pain in the foot. Functional magnetic resonance imaging during brushing of the patient's injured foot showed that tactile allodynia led to activation of several cortical regions including secondary somatosensory cortex, anterior and posterior insular cortex, and anterior cingulate cortex. Brushing of the patient's nonaffected foot led to fewer activated regions. DISCUSSION: The profound sensory disturbances suggest a possible deafferentation type of tactile allodynia mediated by changes within the central nervous system, such as a disruption of normal tactile or thermal inhibition of nociception. The functional magnetic resonance imaging data suggest that tactile allodynia is represented in similar brain regions as experimental pain.     

Right parietal dominance in spatial egocentric discrimination

Egocentric tactile perception is crucial for skilled hand motor control. In order to better understand the brain functional underpinnings related to this basic sensorial perception, we performed a tactile perception functional magnetic resonance imaging (fMRI) experiment with two aims. The first aim consisted of characterizing the neural substrate of two types of egocentric tactile discrimination: the spatial localization (SLD) and simultaneity succession discrimination (SSD) in both hands to define hemispheric dominance for these tasks. The second goal consisted of characterizing the brain activation related to the spatial attentional load, the functional changes and their connectivity patterns induced by the psychometric performance (PP) during SLD. We used fMRI in 25 right-handed volunteers, applying pairs of sinusoidal vibratory stimuli on eight different positions in the palmar surface of both hands. Subjects were required either to identify the stimulus location with respect to an imaginary midline (SLD), to discriminate the simultaneity or succession of a stimuli pair (SSD) or to simply respond to stimulus detection. We found a fronto-parietal network for SLD and frontal network for SSD. During SLD we identified right hemispheric dominance with increased BOLD activation and functional interaction of the right supramarginal gyrus with contralateral intra-parietal sulcus for right and left hand independently. Brain activity correlated to spatial attentional load was found in bilateral structures of intra-parietal sulcus, precuneus extended to superior parietal lobule, pre-supplementary motor area, frontal eye fields and anterior insulae for both hands. We suggest that the right supramarginal gyrus and its interaction with intra-parietal lobule may play a pivotal role in the phenomenon of tactile neglect in right fronto-parietal lesions.     

Dissociating linguistic and nonlinguistic gestural communication in the brain

Gestures of the face, arms, and hands are components of signed languages used by Deaf people. Signaling codes, such as the racecourse betting code known as Tic Tac, are also made up of such gestures. Tic Tac lacks the phonological structure of British Sign Language (BSL) but is similar in terms of its visual and articulatory components. Using fMRI, we compared the neural correlates of viewing a gestural language (BSL) and a manual-brachial code (Tic Tac) relative to a low-level baseline task. We compared three groups: Deaf native signers, hearing native signers, and hearing nonsigners. None of the participants had any knowledge of Tic Tac. All three groups activated an extensive frontal-posterior network in response to both types of stimuli. Superior temporal cortex, including the planum temporale, was activated bilaterally in response to both types of gesture in all groups, irrespective of hearing status. The engagement of these traditionally auditory processing regions was greater in Deaf than hearing participants. These data suggest that the planum temporale may be responsive to visual movement in both deaf and hearing people, yet when hearing is absent early in development, the visual processing role of this region is enhanced. Greater activation for BSL than Tic Tac was observed in signers, but not in nonsigners, in the left posterior superior temporal sulcus and gyrus, extending into the supramarginal gyrus. This suggests that the left posterior perisylvian cortex is of fundamental importance to language processing, regardless of the modality in which it is conveyed.     

Altered central sensorimotor processing in patients with complex regional pain syndrome

Alterations in tactile sensitivity are common in patients with chronic pain. Recent brain imaging studies have indicated that brain areas activated by acute experimental pain partly overlap with areas processing innocuous tactile stimuli. However, the possible effect of chronic pain on central tactile processing has remained unclear. We have examined, both clinically and with whole-head magnetoencephalography, six patients suffering from complex regional pain syndrome (CRPS) of the upper limb. The cortical somatosensory responses were elicited by tactile stimuli applied to the fingertips and the reactivity of spontaneous brain oscillations was monitored as well. Tactile stimulation of the index finger elicited an initial activation at 65 ms in the contralateral SI cortex, followed by activation of the ipsi- and contralateral SII cortices at about 130 ms. The SI responses were 25-55% stronger to stimulation of the painful than the healthy side. The distance between SI representations of thumb and little finger was significantly shorter in the hemisphere contralateral than ipsilateral to the painful upper limb. In addition, reactivity of the 20-Hz motor cortex rhythm to tactile stimuli was altered in the CRPS patients, suggesting modified inhibition of the motor cortex. These results imply that chronic pain may alter central tactile and motor processing.     

静息态功能磁共振成像观察正常人听觉皮层功能

目的 探讨正常人听觉皮层与全脑的正相关及负相关的功能连接.方法 采用静息态下平面回波成像技术采集44名健康受试者fMRI数据,分别以左侧及右侧AⅠ区为种子点,用功能连接的方法观察左、右大脑初级听觉皮层与全脑的正相关及负相关功能连接脑图.结果 分别以双侧AⅠ区为种子点时,正激活的脑网络主要包含双侧AⅠ、AⅡ、岛叶、辅助运动区及扣带回,以同侧为主;与右侧AⅠ区相关的正激活脑区还包括同侧背侧丘脑.与双侧AⅠ区相关的负激活脑网络与脑默认网络大体一致,主要包括双侧后扣带回/楔前叶、额叶内侧回、顶下小叶,双侧小脑半球可见明显激活.结论 静息态磁共振功能连接可满意显示听觉皮层的连接脑图.正相关功能连接主要局限在听觉系统内,负相关功能连接类似于默认网络.     

Putaminal activity is related to perceptual certainty

We have investigated the neural basis of perceptual certainty using a simple discrimination paradigm. Psychophysical experiments have shown that a pair of identical electrical stimuli to the skin or a pair of auditory clicks to the ears are consistently perceived as two separate events in time when the inter-stimulus interval (ISIs) is long, and perceived as simultaneous events when the ISIs are very short. The perceptual certainty of having received one or two stimuli decreases when the ISI lies between these two extremes and this is reflected in inconsistent reporting of the percept across trials. In two fMRI experiments, 14 healthy subjects received either paired electrical pulses delivered to the forearm (ISIs=5-110 ms) or paired auditory clicks presented binaurally (ISIs=1-20 ms). For each subject and modality, we calculated a consistency index (CI) representing the level of perceptual certainty. The task activated pre-SMA and anterior cingulate cortex, plus the cerebellum and the basal ganglia. Critically, activity in the right putamen was linearly dependent on CI for both tactile and auditory discrimination, with topographically distinct effects in the two modalities. These results support a role for the human putamen in the "automatic" perception of temporal features of tactile and auditory stimuli.     

Temporal integration of sequential auditory events: silent period in sound pattern activates human planum temporale

Temporal integration is a fundamental process that the brain carries out to construct coherent percepts from serial sensory events. This process critically depends on the formation of memory traces reconciling past with present events and is particularly important in the auditory domain where sensory information is received both serially and in parallel. It has been suggested that buffers for transient auditory memory traces reside in the auditory cortex. However, previous studies investigating "echoic memory" did not distinguish between brain response to novel auditory stimulus characteristics on the level of basic sound processing and a higher level involving matching of present with stored information. Here we used functional magnetic resonance imaging in combination with a regular pattern of sounds repeated every 100 ms and deviant interspersed stimuli of 100-ms duration, which were either brief presentations of louder sounds or brief periods of silence, to probe the formation of auditory memory traces. To avoid interaction with scanner noise, the auditory stimulation sequence was implemented into the image acquisition scheme. Compared to increased loudness events, silent periods produced specific neural activation in the right planum temporale and temporoparietal junction. Our findings suggest that this area posterior to the auditory cortex plays a critical role in integrating sequential auditory events and is involved in the formation of short-term auditory memory traces. This function of the planum temporale appears to be fundamental in the segregation of simultaneous sound sources.