Neural consequences of somatosensory extinction

There are currently two main interpretations proposing mechanisms underlying tactile extinction: sensory and attention deficit hypotheses. Kinsbourne proposed an opponent processor model to support the attention deficit hypothesis. He insisted that bilateral hemispheres interact reciprocally through contralaterally oriented vectors, and in patients presenting extinction, balance is impaired, causing inattention. From Kinsbourne's point of view, extinction is not caused by sensory disturbance but inattention, therefore even in extinction patients, simultaneous bilateral stimuli should reach the bilateral primary sensory cortices (SI). Using functional magnetic resonance imaging (fMRI), tactile stimuli were administered to both hands of healthy subjects as well as a tactile extinction patient. The patient with tactile extinction extinguished right palm stimuli following simultaneous palm stimulation. During the fMRI study, we gave tactile stimuli to the right palm, the left palm, and simultaneously to both palms. In normal subjects, simultaneous bilateral stimuli activated the bilateral SI and bilateral secondary sensory cortices (SII). In the patient with right tactile extinction, simultaneous bilateral stimuli activated the bilateral SI along with the bilateral SII and right superior parietal lobule. Our study suggests that activation of SI is insufficient to engender an awareness of sensory stimuli. From the view point of Kinsbourne, stimulus driven activity in one hemisphere suppresses activity in the other hemisphere via callosal connections. Our results support the notion that an undamaged superior parietal lobule in the patient with tactile extinction suppresses the damaged parietal lobe function and causes extinction.     

Posterior corpus callosum and interhemispheric transfer of somatosensory information: an fMRI and neuropsychological study of a partially callosotomized patient.

Interhemispheric somatosensory transfer was studied by functional magnetic resonance imaging (fMRI) and neuropsychological tests in a patient who underwent resection of the corpus callosum (CC) for drug-resistant epilepsy in two stages. The first resection involved the anterior half of the body of CC and the second, its posterior half and the splenium. For the fMRI study, the hand was stimulated with a rough sponge. The neuropsychological tests included: Tactile Naming Test (TNT), Same-Different Recognition Test (SDRT), and Tactile Finger Localization Test (intra- and intermanual tasks, TFLT). The patient was studied 1 week before and then 6 months and 1 year after the second surgery. Before this operation, unilateral tactile stimulation of either hand activated contralaterally the first (SI) and second (SII) somatosensory areas and the posterior parietal (PP) cortex, and SII and PP cortex ipsilaterally. All three tests were performed without errors. In both postoperative sessions, somatosensory activation was observed in contralateral SI, SII, and PP cortex, but not in ipsilateral SII and PP cortex. Performance was 100% correct in the TNT for the right hand, but below chance for the left; in the other tests, it was below chance except for TFLT in the intramanual task. This case provides the direct demonstration that activation of SII and PP cortex to stimulation of the ipsilateral hand and normal interhemispheric transfer of tactile information require the integrity of the posterior body of the CC.     

Cooperative processing in primary somatosensory cortex and posterior parietal cortex during tactile working memory

In the present study, causal roles of both the primary somatosensory cortex (SI) and the posterior parietal cortex (PPC) were investigated in a tactile unimodal working memory (WM) task. Individual magnetic resonance imaging‐based single‐pulse transcranial magnetic stimulation (spTMS) was applied, respectively, to the left SI (ipsilateral to tactile stimuli), right SI (contralateral to tactile stimuli) and right PPC (contralateral to tactile stimuli), while human participants were performing a tactile‐tactile unimodal delayed matching‐to‐sample task. The time points of spTMS were 300, 600 and 900 ms after the onset of the tactile sample stimulus (duration: 200 ms). Compared with ipsilateral SI, application of spTMS over either contralateral SI or contralateral PPC at those time points significantly impaired the accuracy of task performance. Meanwhile, the deterioration in accuracy did not vary with the stimulating time points. Together, these results indicate that the tactile information is processed cooperatively by SI and PPC in the same hemisphere, starting from the early delay of the tactile unimodal WM task. This pattern of processing of tactile information is different from the pattern in tactile‐visual cross‐modal WM. In a tactile‐visual cross‐modal WM task, SI and PPC contribute to the processing sequentially, suggesting a process of sensory information transfer during the early delay between modalities.     

BOLD Responses to Tactile Stimuli in Visual and Auditory Cortex Depend on the Frequency Content of Stimulation

Although some brain areas preferentially process information from a particular sensory modality, these areas can also respond to other modalities. Here we used fMRI to show that such responsiveness to tactile stimuli depends on the temporal frequency of stimulation. Participants performed a tactile threshold-tracking task where the tip of either their left or right middle finger was stimulated at 3, 20, or 100 Hz. Whole-brain analysis revealed an effect of stimulus frequency in two regions: the auditory cortex and the visual cortex. The BOLD response in the auditory cortex was stronger during stimulation at hearable frequencies (20 and 100 Hz) whereas the response in the visual cortex was suppressed at infrasonic frequencies (3 Hz). Regardless of which hand was stimulated, the frequency-dependent effects were lateralized to the left auditory cortex and the right visual cortex. Furthermore, the frequency-dependent effects in both areas were abolished when the participants performed a visual task while receiving identical tactile stimulation as in the tactile threshold-tracking task. We interpret these findings in the context of the metamodal theory of brain function, which posits that brain areas contribute to sensory processing by performing specific computations regardless of input modality.     

Brain processing of capsaicin-induced secondary hyperalgesia: a functional MRI study.

OBJECTIVE: To investigate, using functional MRI (fMRI), the neural network that is activated by the pain component of capsaicin-induced secondary mechanical hyperalgesia. BACKGROUND: Mechanical hyperalgesia (i.e., pain to innocuous tactile stimuli) is a distressing symptom of neuropathic pain syndromes. Animal experiments suggest that alterations in central pain processing occur that render tactile stimuli capable of activating central pain-signaling neurons. A similar central sensitization can be produced experimentally with capsaicin. METHODS: In nine healthy individuals the cerebral activation pattern resulting from cutaneous nonpainful mechanical stimulation at the dominant forearm was imaged using fMRI. Capsaicin was injected adjacent to the stimulation site to induce secondary mechanical hyperalgesia. The identical mechanical stimulation was then perceived as painful without changing the stimulus intensity and location. Both activation patterns were compared to isolate the specific pain-related component of mechanical hyperalgesia from the tactile component. RESULTS: The pattern during nonpainful mechanical stimulation included contralateral primary sensory cortex (SI) and bilateral secondary sensory cortex (SII) activity. During hyperalgesia, significantly higher activation was found in the contralateral prefrontal cortex: the middle (Brodmann areas [BAs] 6, 8, and 9) and inferior frontal gyrus (BAs 44 and 45). No change was present within SI, SII, and the anterior cingulate cortex. CONCLUSIONS: Prefrontal activation is interpreted as a consequence of attention, cognitive evaluation, and planning of motor behavior in response to pain. The lack of activation of the anterior cingulate contrasts with physiologic pain after C-nociceptor stimulation. It might indicate differences in the processing of hyperalgesia and C-nociceptor pain or it might be due to habituation of affective sensations during hyperalgesia compared with acute capsaicin pain.     

Event-related fMRI of the somatosensory system using electrical finger stimulation

Cortical signal intensity changes due to brief (1 s) innocuous electrical stimuli applied to the second and fifth finger of the right hand were measured by means of fMRI at 1.5 T. The activation pattern in this event-related fMRI approach closely resembled that obtained in recent block-design studies. Activations were found in contralateral primary (SI) and bilaterally in secondary (SII) somato-sensory cortex as well as in posterior parietal cortex, insula, and supplementary motor area (SMA). In SI, the somatotopic organization of the hand area is demonstrated, more clearly to be seen in area 3b than in area 1 and 2. In conclusion, the feasibility to employ event-related somatosensory stimulation paradigms in fMRI studies is demonstrated.     

Tactile awareness and limb position in neglect: functional magnetic resonance imaging

We studied a patient with right parietal damage for whom tactile stimuli on the right/ipsilesional hand (projecting to the intact left hemisphere) were extinguished from awareness during double simultaneous stimulation, when his right hand was positioned in the left/contralesional space. This demonstrates the role of an egocentric spatial reference frame in attention that can determine awareness of stimuli despite intact sensory pathways. Using functional magnetic resonance imaging to elucidate the neural correlates of such perceptual extinction, we found that limb position modulated neural responses to tactile stimuli at early cortical stages (SI) in the intact hemisphere. Activity in bilateral middle frontal gyri also was modulated by limb position and may contribute to integrate sensory inputs into a supramodal, egocentric representation of space.     

Neural correlates of an illusory touch experience investigated with fMRI

When asked to judge the presence or absence of near-threshold tactile stimuli, participants often report touch experiences when no tactile stimulation has been delivered (‘false alarms’). The simultaneous presentation of a light flash during the stimulation period can increase the frequency of touch reports, both when touch is and is not present. Using fMRI, we investigated the BOLD response during both light-present and light-absent false alarms, testing predictions concerning two possible neural mechanisms underlying these illusory touch experiences: activation of a tactile representation in primary somatosensory cortex (SI) and/or activation of a tactile representation in late processing areas outside of sensory-specific cortex, such as medial prefrontal cortex (MPC). Our behavioural results showed that participants made false alarms in light-present and light-absent trials, both of which activated regions of the medial parietal and medial prefrontal cortex including precuneus, posterior cingulate and paracingulate cortex, suggesting the same underlying mechanism. However, only a non-significant increase in SI activity was measured in response to false alarm vs. correct rejection trials. We argue that our results provide evidence for the role of top-down regions in somatic misperception, consistent with findings from studies in humans and non-human primates.     

Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation--an fMRI study.

OBJECTIVE: Ten healthy adult subjects were examined using functional magnetic resonance imaging (fMRI) to investigate responses in the contralateral and ipsilateral primary somatosensory cortex (SI) following electrical stimulation of the median nerve. METHODS: The right and left median nerves were stimulated alternately at the wrist in the different sessions. First, the location of the response in contralateral SI was identified following median nerve stimulation, and then, a spherical search volume with a 10mm radius centered on the region of the contralateral response was determined. Whether or not fMRI activation occurred within this sphere following ipsilateral stimulation was examined using a 3T MR imager. RESULTS: A response in contralateral SI was observed in 8 of the 10 subjects in right and left hemisphere. Responses in ipsilateral SI were observed in 6 of 8 subjects in right hemisphere, and the region of the response tended to be posterior to the contralateral region. On the other hand, in left hemisphere, the ipsilateral responses were found in three. CONCLUSIONS: In the present study, not only contralateral SI but also ipsilateral SI was activated following median nerve. The location of the ipsilateral activation was significantly more posterior than the contralateral one in right hemisphere. SIGNIFICANCE: The region of activation in ipsilateral SI was located in the posterior portion of post central gyrus, corresponding to around BA2 and 5 in human.     

Short communication: mapping of somatosensory cortices with functional magnetic resonance imaging in anaesthetized macaque monkeys

Functional magnetic resonance imaging (fMRI) in macaque monkeys is emerging as a potent candidate to bridge the gap between data from human fMRI studies and data from anatomy, electrophysiology and lesion studies in monkeys. The primary (SI) and secondary (SII) somatosensory cortices are the principal regions for somatosensory information processing and contain systematic representations of the body surface map (somatotopy). To examine the functional organization of the somatosensory cortices in anaesthetized macaque monkeys with fMRI, we asked whether focal and differential activation could be observed in SI and SII in response to tactile stimulation with two parameters: body sides (right and left) and body regions (hand and face). We found that changes in stimulus parameters elicited differential focal activation in both SI and SII in two ways. First, the hand and face stimulation activated SI and SII in the contralateral, but not in the ipsilateral, hemisphere. Second, the hand and face stimulation differentially activated two adjacent regions in both SI and SII. These fMRI results appear to correlate with previous mapping studies by other methods in the macaque somatosensory cortices. This study shows the feasibility of fMRI studies in mapping multiple sensory areas in monkeys by which we can distinguish between adjacent functionally distinct regions.     

Direct current stimulation over the human sensorimotor cortex modulates the brain's hemodynamic response to tactile stimulation

Tactile stimuli produce afferent signals that activate specific regions of the cerebral cortex. Noninvasive transcranial direct current stimulation (tDCS) effectively modulates cortical excitability. We therefore hypothesised that a single session of tDCS targeting the sensory cortices would alter the cortical response to tactile stimuli. This hypothesis was tested with a block‐design functional magnetic resonance imaging protocol designed to quantify the blood oxygen level‐dependent response to controlled sinusoidal pressure stimulation applied to the right foot sole, as compared with rest, in 16 healthy young adults. Following sham tDCS, right foot sole stimulation was associated with activation bilaterally within the precentral cortex, postcentral cortex, middle and superior frontal gyri, temporal lobe (subgyral) and cingulate gyrus. Activation was also observed in the left insula, middle temporal lobe, superior parietal lobule, supramarginal gyrus and thalamus, as well as the right inferior parietal lobule and claustrum (false discovery rate corrected, P < 0.05). To explore the regional effects of tDCS, brain regions related to somatosensory processing, and cortical areas underneath each tDCS electrode, were chosen as regions of interest. Real tDCS, as compared with sham tDCS, increased the percent signal change associated with foot stimulation relative to rest in the left posterior paracentral lobule. These results indicate that tDCS acutely modulated the cortical responsiveness to controlled foot pressure stimuli in healthy adults. Further study is warranted, in both healthy individuals and patients with sensory impairments, to link tDCS‐induced modulation of the cortical response to tactile stimuli with changes in somatosensory perception.     

Continuous theta-burst rTMS over primary somatosensory cortex modulates tactile perception on the hand

ObjectiveTheta-burst stimulation (TBS) over the primary somatosensory cortex (SI) alters cortical excitability, and in its intermittent form (iTBS) improves tactile spatial acuity. The effects of continuous TBS (cTBS) on tactile acuity remain unknown. The present study examined the influence of cTBS over SI on temporal and spatial tactile acuity on the contralateral hand.MethodsIn separate experiments, temporal discrimination threshold (TDT) and spatial amplitude discrimination threshold (SDT) were obtained from the right hand before and for up to 34 min following real and sham cTBS (600 pulses) over left-hemisphere SI.ResultsCTBS reduced temporal and spatial tactile acuity for up to 18 min following real cTBS. Tactile acuity was unaltered in the groups receiving sham cTBS.ConclusionsCTBS over SI impairs both temporal and spatial domains of tactile acuity for a similar duration.SignificanceCTBS over SI appears to decrease neural activity within targeted cortex and has potential utility in reducing excessive sensory processing.     

Aberrant cortical functionality and somatosensory deficits after stroke.

Damage and/or disconnection of the primary somatosensory cortex (SI) after stroke leads to deficits in touch perception. We used magnetoencephalography to test whether specific patterns of functionality of the somatosensory cortex are associated with different degrees of postacute somatosensory deficit. Nineteen postacute unilateral stroke patients suffering different degrees of somatosensory deficit (six nonexistent, six moderate, and seven severe) and eight aged-matched controls underwent high-resolution MRI and whole-head magnetoencephalography recordings of somatosensory-evoked fields and of spontaneous slow oscillatory activity. Amplitude of SI activation after tactile stimulation in the affected and nonaffected hemispheres and delta dipole density (DDD) in the postcentral areas were estimated and compared across the four groups. Severe postacute somatosensory deficit was accompanied, in all cases, with absence of SI responses to stimulation in the affected hand and a significant asymmetry in postcentral DDD toward the affected hemisphere. Patients with moderate sensory loss showed asymmetry in their postcentral DDD (four cases toward the affected hemisphere and two toward the unaffected) but no atypical amplitudes in SI activation. Recordings in stroke patients without somatosensory deficit did not differ from those obtained in controls for SI amplitude or postcentral DDD. In stroke patients, amplitude of SI responses and postcentral DDD show a negative correlation. Lack of activation of SI cortex after stimulation of the affected hand and spontaneous slow oscillatory activity in postcentral areas are neurophysiological correlates of somatosensory deficit in the postacute phase of stroke.     

Neural activity related to self- versus externally generated painful stimuli reveals distinct differences in the lateral pain system in a parametric fMRI study

Self-generated sensory stimulation can be distinguished from externally generated stimulation that is otherwise identical. To determine how the brain differentiates external from self-generated noxious stimulation and which structures of the lateral pain system use neural signals to predict the sensory consequences of self-generated painful stimulation, we used functional magnetic resonance imaging to examine healthy human subjects who received thermal-contact stimuli with noxious and non-noxious temperatures on the resting right hand in random order. These stimuli were internally (self-generated) or externally generated. Two additional conditions served as control conditions: to account for stimulus onset uncertainty, acoustic stimuli preceding the same thermal stimuli were used with variable or fixed delays but without any stimulus-eliciting movements. Whereas graded pain-related activity in the insula and secondary somatosensory cortex (SII) was independent of how the stimulus was generated, it was attenuated in the primary somatosensory cortex (SI) during self-generated stimulation. These data agree with recent concepts of the parallel processing of nociceptive signals to the primary and secondary somatosensory cortices. They also suggest that brain areas that encode pain intensity do not distinguish between internally or externally applied noxious stimuli, i.e., this adaptive biological mechanism prevents harm to the individual. The attenuated activation of SI during self-generated painful stimulation might be a result of the predictability of the sensory consequences of the pain-related action.     

The space of senses: impaired crossmodal interactions in a patient with Balint syndrome after bilateral parietal damage

Balint syndrome after bilateral parietal damage involves a severe disturbance of space representation including impaired oculomotor behaviour, optic ataxia, and simultanagnosia. Binding of object features into a unique spatial representation can also be impaired. We report a patient with bilateral parietal lesions and Balint syndrome, showing severe spatial deficits in several visual tasks predominantly affecting the left hemispace. In particular, we tested whether a loss of spatial representation would affect crossmodal interactions between simultaneous visual and tactile events occurring at the same versus different locations. A tactile discrimination task, where spatially congruent or incongruent visual cues were delivered near the patient's hands, was used. Following stimulation of the left hand in the left side of space, we observed visuo-tactile interactions that were not modulated by spatially congruent conditions. In contrast, performance following stimulation of the right hand in the right side of space was affected in a spatially selective manner--facilitated for congruent stimuli and slowed for incongruent stimuli. To dissociate effects on somatotopic and spatiotopic coordinates, we crossed the patient's hands during unimodal tactile discriminations. Tactile performance of the left hand improved when it was positioned in the right hemispace, whereas placing the right hand in left space produced no significant changes, suggesting that left-sided tactile inputs are coded with respect to a combination of limb- and trunk-centred coordinates. These data converge with recent findings in animals and healthy humans to indicate a critical role of the posterior parietal cortex in multimodal spatial integration, and in the fusion of different coordinates into a unified representation of space.     

Effects of co-activation on cortical organization and discrimination performance

We used fMRI to investigate the effects of tactile co-activation on the topographic organization of the human primary somatosensory cortex (SI). Behavioral consequences of co-activation were studied in a psychophysical task assessing the mislocalization of tactile stimuli. Co-activation was applied to the index, middle and ring fingers of the right hand either synchronously or asynchronously. Cortical representations for synchronously co-activated fingers moved closer together, whereas cortical representations for asynchronously co-activated fingers became segregated. Behaviorally, this pattern coincided with an increased and reduced number of mislocalizations between synchronously and asynchronously co-activated fingers, respectively. Thus, both synchronous and asynchronous coupling of passive tactile stimulation is able to induce short-term cortical reorganization associated with functionally relevant changes.     

Effects of visual information regarding tactile stimulation on the somatosensory cortical activation:a functional MRI study

Many studies have investigated the evidence for tactile and visual interactive responses to activation of various brain regions. However, few studies have reported on the effects of visuo-tactile multisensory inte-gration on the amount of brain activation on the somatosensory cortical regions. The aim of this study was to examine whether coincidental information obtained by tactile stimulation can affect the somatosensory cortical activation using functional MRI. Ten right-handed healthy subjects were recruited for this study. Two tasks (tactile stimulation and visuotactile stimulation) were performed using a block paradigm during fMRI scanning. In the tactile stimulation task, in subjects with eyes closed, tactile stimulation was applied on the dorsum of the right hand, corresponding to the proximal to distal directions, using a rubber brush. In the visuotactile stimulation task, tactile stimulation was applied to observe the attached mirror in the MRI chamber reflecting their hands being touched with the brush. In the result of SPM group analysis, we found brain activation on the somatosensory cortical area. Tactile stimulation task induced brain acti-vations in the left primary sensory-motor cortex (SM1) and secondary somatosensory cortex (S2). In the visuo-tactile stimulation task, brain activations were observed in the both SM1, both S2, and right posterior parietal cortex. In all tasks, the peak activation was detected in the contralateral SM1. We examined the ef-fects of visuo-tactile multisensory integration on the SM1 and found that visual information during tactile stimulation could enhance activations on SM1 compared to the tactile unisensory stimulation.     

Characterization of cortical hemodynamic changes following sensory,visual, and speech activation by intraoperative optical imaging utilizing phase‐based evaluation methods

Alterations within cerebral hemodynamics are the intrinsic signal source for a wide variety of neuroimaging techniques. Stimulation of specific functions leads due to neurovascular coupling, to changes in regional cerebral blood flow, oxygenation and volume. In this study, we investigated the temporal characteristics of cortical hemodynamic responses following electrical, tactile, visual, and speech activation for different stimulation paradigms using Intraoperative Optical Imaging (IOI). Image datasets from a total of 22 patients that underwent surgical resection of brain tumors were evaluated. The measured reflectance changes at different light wavelength bands, representing alterations in regional cortical blood volume (CBV), and deoxyhemoglobin (HbR) concentration, were assessed by using Fourier‐based evaluation methods. We found a decrease of CBV connected to an increase of HbR within the contralateral primary sensory cortex (SI) in patients that were prolonged (30 s/15 s) electrically stimulated. Additionally, we found differences in amplitude as well as localization of activated areas for different stimulation patterns. Contrary to electrical stimulation, prolonged tactile as well as prolonged visual stimulation are provoking increases in CBV within the corresponding activated areas (SI, visual cortex). The processing of the acquired data from awake patients performing speech tasks reveals areas with increased, as well as areas with decreased CBV. The results lead us to the conclusion, that the CBV decreases in connection with HbR increases in SI are associated to processing of nociceptive stimuli and that stimulation type, as well as paradigm have a nonnegligible impact on the temporal characteristics of the following hemodynamic response.     

Hand somatosensory cortex activity following selective dorsal rhizotomy: report of three cases with fMRI

Introduction Selective dorsal rhizotomy (SDR) is an effective treatment for lower extremity spasticity in cerebral palsy. Cortical organization in sensory cortex may be abnormal in cerebral palsy, and deafferentation is known to lead to cortical reorganization in many situations.Methods We used functional magnetic resonance imaging (fMRI) of hand sensory stimulation to determine if the partial deafferentation of the lower extremity sensory system, associated with SDR, led to any alterations in the cortical somatosensory representation for the upper limbs. Three patients with spastic diplegia were studied with blood oxygen level-dependent (BOLD)-fMRI before and after SDR. fMRI during tactile stimulation of the digits of the right hand was used to map hand somatosensory cortex. Comparison of the cortical maps devoted to the hand before and after SDR assessed for cortical reorganization following partial deafferentation of the lower extremity.Results In the one patient with upper extremity involvement, the hand sensory representation was markedly enhanced following SDR. In the other two patients, a normal pattern, but with diminished activity, was seen compared with preoperative findings. SDR for lower limb spastic diplegia does not lead to extensive reorganization of cortex dedicated to the representation of the upper limb. An essentially normal pattern of activation was seen both before and after SDR.Conclusion The relief of attention demands associated with spasticity may explain the modulation in intensity seen after SDR in the patients who exhibited no upper extremity involvement despite lower limb spasticity.     

Human brain activation during sexual stimulation of the penis

Penile sensory information is essential for reproduction, but almost nothing is known about how sexually salient inputs from the penis are processed in the brain. We used positron emission tomography to measure regional cerebral blood flow (rCBF) during various stages of male sexual performance. Compared to a passive resting condition (without penile erection), sexual stimulation of the penis increased rCBF in an area of the right hemisphere encompassing the posterior insula and adjacent posterior part of the secondary somatosensory cortex (SII) and decreased rCBF in the right amygdala. No activation was observed in either the thalamus, genital part of primary somatosensory cortex (SI), or hypothalamus. Based on these results we put forward the concept that during sexual performance the salience of the stimulus, represented by activation of the insula and SII, is of greater significance than the exact location of the stimulus, encoded in SI. The absence of activation in the hypothalamus indicates that this region is more important for the onset of sexual arousal than for the resulting sexual performance. Deactivation of the amygdala during sexual stimulation of the penis corresponds with a decrease of vigilance during sexual performance.