Role of human SII cortices in sensorimotor integration.

OBJECTIVES: To elucidate the functional properties of neurons in the human primary (SI) and ipsilateral and contralateral secondary (iSII or cSII) cortices in response to stimuli during finger movement.METHODS: We measured somatosensory evoked fields (SEFs) produced by electric stimuli delivered to the median nerve at 0.2 Hz in 6 healthy subjects.RESULTS: The amplitudes of evoked fields from both iSII and cSII were gradually attenuated with time. Consecutive blocks of trials were obtained to assess the habituation of each evoked field. Complex finger movements with attention (gating session) increased the amplitude of evoked fields from the iSII cortices but reduced the amplitudes of evoked fields from the cSII cortices (P<0.01). In contrast, the amplitude of P30 m from the SI did not show habituation effects but decreased significantly in the gating session (P<0.01).CONCLUSIONS: The enhanced iSII as well as suppressed cSII cortices during complex finger movements with attention are not only considered to be result of gating effect but also attention.     

Effects of movement on somatosensory N20m fields and high-frequency oscillations

Somatosensory evoked fields were recorded to determine the effects of movement and attention on high-frequency oscillations during active finger movements of the ipsilateral and contralateral sides in response to electrical stimulation of the median nerve. A whole-scalp neuromagnetometer was used to record somatosensory evoked fields from eight subjects following electric median nerve stimulation at the wrist. The following three sessions were performed: (1). rest, (2). movement of fingers on the ipsilateral in response to stimulation and (3). movement of fingers on the contralateral in response to stimulation. The somatosensory evoked fields with a wide-bandpass (0.1-1000 Hz) were recorded. High-frequency oscillations and N20m were separated by subsequent high-pass (> 300 Hz) and low-pass (< 300 Hz) filtering. The maximum amplitude of high-frequency oscillations decreased during finger movements accompanying a decrease in somatosensory N20m dipole strength. Activation of the motor cortex appeared to suppress both the amplitude of high-frequency oscillations and the N20m dipole strength.     

Second somatosensory area (SII) plays a significant role in selective somatosensory attention

In order to explore human cortical areas involved in active attention toward a somatosensory modality, somatosensory evoked cortical magnetic fields were recorded in ten healthy adults with a 122-channel whole-head magnetometer while the subjects performed the selective attention task. Two kinds of stimulus modality, somatosensory and auditory, were presented independently in the same session. For the somatosensory modality, a randomized sequence of strong (P=0.45) and weak (P=0.05) electric stimuli was delivered to the right median nerve at the wrist. For the auditory modality, a randomized sequence of 900-Hz (P=0.45) and 950-Hz (P=0.05) tones was delivered to both ears. Subjects were requested to pay attention to the specified stimulus modality (either somatosensory or auditory) and to count the number of rare stimuli of the attended modality (weak stimuli in the somatosensory or 950-Hz tone in the auditory modality). A total of 12 sessions were performed for each subject, among which the order of attended modality was changed alternately and counterbalanced among subjects. In the data analysis, somatosensory evoked fields for frequent stimuli (strong electric stimuli) were compared between the two conditions; attend somatosensory condition (ATS) and attend auditory condition (non-attend somatosensory condition; NATS). In six out of the ten subjects, somatosensory evoked fields showed attention-related change. The magnitude of the estimated generator source in SII, but not in SI, significantly increased from NATS to ATS while keeping the same locations. Moreover, a simulation study using the estimated sources in SII in NATS supported the enhancement of the activity in the SII rather than participation of additional sources in the selective attention task. These results suggest that the SII plays a main role in selective somatosensory attention.     

Cerebral magnetic responses to stimulation of ulnar and median nerves

We have compared spatial patterns of somatosensory evoked magnetic fields (SEFs) to stimulation of the ulnar and median nerves at the wrist. An oddball paradigm was used additionally to examine whether an infrequent change in the stimulation site would alter the field pattern. The response consisted of 3 parts: an early small deflection at 22-28 msec, a large deflection peaking between 34 and 86 msec, and a late deflection at 110-180 msec. The wave forms and amplitudes of the responses to ulnar and median nerve stimulation were similar, without any additional deflections for the infrequent stimuli. The field patterns, which were interpreted in terms of the dipole model, could be explained by activation of the primary sensorimotor cortex during all peaks of the response. For the early parts of the response at 22-46 msec, the locations of the equivalent sources for median and ulnar nerve stimulation differed from each other, in agreement with the known somatotopy of SI. No somatotopical order was found for the sources of the later deflections.     

Dorsal penile nerve stimulation elicits left-hemisphere dominant activation in the second somatosensory cortex

Activation of peripheral mixed and cutaneous nerves activates a distributed cortical network including the second somatosensory cortex (SII) in the parietal operculum. SII activation has not been previously reported in the stimulation of the dorsal penile nerve (DPN). We recorded somatosensory evoked fields (SEFs) to DPN stimulation from 7 healthy adults with a 122-channel whole-scalp neuromagnetometer. Electrical pulses were applied once every 0.5 or 1.5 sec to the left and right DPN. For comparison, left and right median and tibial nerves were stimulated alternatingly at 1.5-sec intervals. DPN stimuli elicited weak, early responses in the vicinity of responses to tibial nerve stimulation in the primary somatosensory cortex. Strong later responses, peaking at 107-126 msec were evoked in the SII cortices of both hemispheres, with left-hemisphere dominance. In addition to tactile processing, SII could also contribute to mediating emotional effects of DPN stimuli.     

Short latency mechanically evoked somatosensory potentials in humans.

Somatosensory potentials evoked by mechanical stimulation were recorded by surface electrodes over (1) the digital nerves in the index finger, (2) the median nerve at the wrist, (3) the median nerve near the axilla, (4) the brachial plexus, (5) the cervical cord at CII, (6) the scalp overlying the somatosensory cortex. Nerve conduction velocities varied inversely with age and ranged from 43 to 68 m/sec. Mechanically evoked potentials recorded from the electrodes overlying the digital nerves were an artifact of the finger movement. All other electrode configurations recorded potentials comparable to those evoked by electrical stimulation of nerves. These mechanically evoked potentials could prove useful in the assessment of clinical disorders of somatosensory function from receptor to cortex in man.     

Sensorimotor integration in human primary and secondary somatosensory cortices

We measured somatosensory evoked fields (SEFs) to electric median nerve stimuli from eight healthy subjects with a whole-scalp 122-channel neuromagnetometer in two different conditions: (i) ‘rest', with stimuli producing clear tactile sensation without any motor movement, and (ii) ‘contraction' with exactly the same stimuli as in ‘rest', but with the subjects maintaining sub-maximal isometric contraction in thenar muscles of the stimulated hand. The aim was to study the role of the primary (SI) and secondary somatosensory (SII) cortices in sensorimotor integration. The amplitude of the SI response N20m did not change with coincident isometric contraction, whereas P35m was significantly reduced. On the contrary, activation of contra- and ipsilateral SII cortices was significantly enhanced during the contraction. We suggest that isometric contraction facilitates activation of SII cortices to tactile stimuli, possibly by decreasing inhibition from the SI cortex. The enhanced SII activation may be related to tuning of SII neurons towards relevant tactile input arising from the region of the body where the muscle activation occurs.     

Selectivity of attenuation (i.e., gating) of somatosensory potentials during voluntary movement in humans

Attenuation of somatosensory evoked potentials (SEPS) recorded from the scalp during voluntary movement occurs for specific combinations of the finger moved and the peripheral nerve stimulated. The cerebral potential component occurring at a latency of 27 msec (P27) evoked either by stimulation of median nerve at the wrist or by stimulation of 1st and 2nd digit nerves in the fingers were selectively attenuated during movement of 1st digit but were not altered during movement of 5th digit. By contrast, the cerebral P27 component evoked by stimulation of ulnar nerve at the wrist or by stimulation of 5th digital nerve were attenuated during movement of that digit but were not altered during movement of 1st digit. Gating of somatosensory activity is a selective phenomenon occurring when movement involves the areas being stimulated.     

Somatosensory evoked potential recovery in kii amyotrophic lateral sclerosis/parkinsonism-dementia complex (kii AlS/PDC).

OBJECTIVE: To evaluate the recovery function of the sensory cortex in patients with Kii amyotrophic lateral sclerosis/parkinsonism-dementia complex (Kii ALS/PDC) using somatosensory evoked potentials (SEPs) elicited by paired stimuli of the median nerve at the wrist. METHODS: Five patients with Kii ALS/PDC were compared with 5 patients with classical ALS, 5 with Parkinson's disease (PD), and 7 healthy normal volunteers. SEPs were recorded from the hand sensory area contralateral to the side of stimulation. Recovery functions of N20-P25 and P25-N33 components were evaluated by comparing the second SEPs elicited by paired pulse stimuli at various interstimulus intervals (ISIs, 20-300 ms) with the SEPs elicited by single stimuli. RESULTS: Conventional SEPs to a single stimulus had a normal latency and size in all patients. The recovery function of the N20-P25 and P25-N33 components showed significantly less suppression at short ISIs without any facilitation at long ISIs in Kii ALS/PDC patients than in normal subjects, classical ALS or PD patients. CONCLUSIONS: In Kii ALS/PDC, the sensory cortex is disinhibited or hyperexcitable. These abnormalities may reflect cortical pathology in the sensory cortex and may be partly due to a secondary effect on the sensory cortex from the primary parkinsonian pathological changes.     

Topographic organization of the human primary and secondary somatosensory areas: an fMRI study

The topographical organization of SI and SII somatosensory areas was investigated using fMRI at 1.5 T and electrical sensory stimulation. Electrical stimuli were delivered unilaterally to the median nerve at the wrist and to the tibial nerve at the medial malleolus, during a block paradigm study. In all subjects, activation was observed, contralaterally to the stimulated side, in the post-central gyrus, in the posterior parietal cortex, in the mesial pre-frontal region and, bilaterally, in the supratemporal region at the level of the Sylvian fissure. The latter region, corresponding presumably to SII, showed a rough but clearcut topographical organization, with the median nerve areas located more posteriorly. In addition, weaker activations were observed in some subjects in the ipsilateral mesial prefrontal region and in the ipsilateral posterior parietal cortex. Information contained in the present study represent an interesting database for future investigations on the effects of sensorimotor learning in normal individuals on plastic reorganization following a lesion of the primary sensorimotor centers, i.e. in stroke patients, on the topography and balance between upper and lower limb representations in primary and secondary somatosensory cortices.     

Lack of activation of human secondary somatosensory cortex in Unverricht-Lundborg type of progressive myoclonus epilepsy

Previous electroencephalographic and magnetoencephalographic studies have demonstrated giant early somatosensory cortical responses in patients with cortical myoclonus. We applied whole-scalp magnetoencephalography to study activation sequences of the somatosensory cortical network in 7 patients with Unverricht-Lundborg-type progressive myoclonus epilepsy diagnostically verified by DNA analysis. Responses to electric median nerve stimuli displayed 30-msec peaks at the contralateral primary somatosensory cortex that were four times stronger in patients than in control subjects. The amplitudes of 20-msec responses did not significantly differ between the groups. In contrast to control subjects, 5 patients displayed ipsilateral primary somatosensory cortex activity at 48 to 61 msec in response to both left- and right-sided median nerve stimuli. Furthermore, their secondary somatosensory cortex was not significantly activated. These abnormalities indicate altered responsiveness of the entire somatosensory cortical network outside the contralateral primary somatosensory cortex in patients with Unverricht-Lundborg-type progressive myoclonus epilepsy. The deficient activation of the secondary somatosensory cortex in Unverricht-Lundborg patients may reflect disturbed sensorimotor integration, probably related to impaired movement coordination.     

Spatiotemporal dynamics of bimanual integration in human somatosensory cortex and their relevance to bimanual object manipulation

Little is known about the spatiotemporal dynamics of cortical responses that integrate slightly asynchronous somatosensory inputs from both hands. This study aimed to clarify the timing and magnitude of interhemispheric interactions during early integration of bimanual somatosensory information in different somatosensory regions and their relevance for bimanual object manipulation and exploration. Using multi-fiber probabilistic diffusion tractography and MEG source analysis of conditioning-test (C-T) median nerve somatosensory evoked fields in healthy human subjects, we sought to extract measures of structural and effective callosal connectivity between different somatosensory cortical regions and correlated them with bimanual tactile task performance. Neuromagnetic responses were found in major somatosensory regions, i.e., primary somatosensory cortex SI, secondary somatosensory cortex SII, posterior parietal cortex, and premotor cortex. Contralateral to the test stimulus, SII activity was maximally suppressed by 51% at C-T intervals of 40 and 60 ms. This interhemispheric inhibition of the contralateral SII source activity correlated directly and topographically specifically with the fractional anisotropy of callosal fibers interconnecting SII. Thus, the putative pathway that mediated inhibitory interhemispheric interactions in SII was a transcallosal route from ipsilateral to contralateral SII. Moreover, interhemispheric inhibition of SII source activity correlated directly with bimanual tactile task performance. These findings were exclusive to SII. Our data suggest that early interhemispheric somatosensory integration primarily occurs in SII, is mediated by callosal fibers that interconnect homologous SII areas, and has behavioral importance for bimanual object manipulation and exploration.     

Somatotopic representation of the tongue in human secondary somatosensory cortex

OBJECTIVE: To clarify the somatotopic representation of the tongue secondary somatosensory cortex (SII) in humans. METHODS: Somatosensory evoked magnetic fields (SEFs) were recorded from nine subjects after stimulating four body sites, left antero (LA) and postero (LP) lateral margins of the tongue, left median nerve at the wrist (Hand), and left tibial nerve at the ankle (Foot). RESULTS: Clear neural activities were recorded from the bilateral SII in both hemispheres after the four sites were stimulated. The tongue SII for LA and LP was located close to the hand SII and significantly more anterior than the Foot SII. There was no significant difference in the location of dipoles between the LA and LP areas of the tongue SII. The mean peak latencies of the tongue SII for LA and LP were significantly shorter in the hemisphere contralateral to the stimulation than the ipsilateral hemisphere. CONCLUSIONS: The tongue areas are considered to occupy a small region in SII with insufficient spatial separation to differentiate anterior from posterior areas even using magnetoencephalography which has a higher spatial resolution than electroencephalography (EEG). SIGNIFICANCE: This is the first systematical study to clarify the activated regions in SII following stimulation of the tongue.     

Interaction of afferent impulses in the human primary sensorimotor cortex.

We recorded somatosensory evoked magnetic fields (SEFs) over the hand area of the primary sensorimotor cortex (SMI) in 6 healthy adults in 2 sets of experiments to study interaction of afferent impulses. In experiment 1, SEFs were elicited by contralateral median nerve (MC) stimuli presented alone and 40 msec after a conditioning stimulus to the contralateral ulnar (UC), ipsilateral median (MI) or contralateral tibial (TC) nerve. N20m, P30m and P60m deflections to MC stimulation were markedly attenuated by preceding UC stimulation whereas N40m was enhanced, and a novel P80m emerged. In contrast, MI or TC stimulation did not affect the responses to MC. In experiment 2, the time course of recovery of N20m to median nerve stimuli was studied after stimulation of the adjacent ulnar and of the same median nerve. The recovery curves were similar for both conditioning stimuli with nearly full recovery of N20m at 120 msec. The results indicate marked interaction of impulses from ipsilateral median and ulnar nerves in human SMI, but no evidence was found of interaction from the two hands or from ipsilateral hand and foot.     

Effect of transcranial DC sensorimotor cortex stimulation on somatosensory evoked potentials in humans.

OBJECTIVE: To study the after-effect of transcranial direct current stimulation (tDCS) over the sensorimotor cortex on the size of somatosensory evoked potentials (SEPs) in humans. METHODS: SEPs were elicited by electrical stimulation of right or left median nerve at the wrist before and after anodal or cathodal tDCS in 8 healthy subjects. tDCS was applied for 10 min to the left motor cortex at a current strength of 1 mA. RESULTS: Amplitudes of P25/N33, N33/P40 (parietal components) and P22/N30 (frontal component) following right median nerve stimulation were significantly increased for at least 60 min after the end of anodal tDCS, whereas P14/N20, N20/P25 (parietal components) and N18/P22 (frontal component) were unaffected. There was no effect on SEPs evoked by left median nerve stimulation. Cathodal tDCS had no effect on SEPs evoked from stimulation of either arm. CONCLUSIONS: Anodal tDCS over the sensorimotor cortex can induce a long-lasting increase in the size of ipsilateral cortical components of SEPs. SIGNIFICANCE: tDCS can modulate cortical somatosensory processing in humans and might be a useful tool to induce plasticity in cortical sensory processing.     

Changes in median nerve somatosensory transmission and motor output following transient deafferentation of the radial nerve in humans.

OBJECTIVE: To determine if transient anaesthetic deafferentation of the radial nerve would lead to alterations in processing of early somatosensory evoked potentials (SEPs) from the median nerve or alter cortico-motor output to the median nerve innervated abductor pollicis brevis (APB) muscle. METHODS: Spinal, brainstem, and cortical SEPs to median nerve stimulation were recorded before, during and after ipsilateral radial nerve block with local anaesthesia. Motor evoked potentials (MEPs) and motor cortex output maps were recorded from the APB muscle. RESULTS: There were no significant changes to most early SEP peaks. The N30 peak, however, showed a significant increase in amplitude, which remained elevated throughout the anaesthetic period, returning to baseline once the anaesthetic had completely worn off. MEP amplitude of the median nerve innervated APB muscle was significantly decreased during the radial nerve blockade. There was also a significant alteration in the APB optimal site location, and a small but significant decrease in the silent period during the radial nerve blockade. CONCLUSIONS: Transient anaesthetic deafferentation of the radial nerve at the elbow leads to a rapid modulation of cortical processing of median nerve input and output. These changes suggest an overall decrease in motor cortex output to a median nerve innervated muscle not affected by the radial nerve block, occurring concomitantly with an increased amplitude of the median nerve generated N30 SEP peak, thought to represent processing in the supplementary motor area (SMA). Independent subcortical connections to the SMA are thought to contribute to the N30 response observed in this study. Unmasking of pre-existing but latent cortico-cortical and/or thalamo-cortical connections may be the mechanism underlying the cortical SEP increases observed following radial nerve deafferentation. SIGNIFICANCE: Transient deafferentation of the radial nerve, which supplies wrist and hand extensor muscles, has been shown to alter sensory processing from and motor output to the median nerve innervated thenar muscles.     

‘Gating’ of somatosensory evoked potentials begins before the onset of voluntary movement in man

The inflow of somatosensory information to the cerebral cortex is modified before and during active movement in animals. This phenomenon has been termed ‘gating’ and occurs at several levels of the sensory pathway. We studied somatosensory evoked potentials (SEPs) to stimulation of the median nerve at the wrist during voluntary movement of the ipsilateral thumb in man. Results indicate that SEPs are attenuated shortly after a command to move (approximately 100 ms before the onset of the electromyogram (EMG)), become maximally attenuated with maximum EMG and return to normal size when movement is finished.     

Effects of passive tactile co-activation on median ulnar nerve representation in human SI

In animals simple passive co-activation causes a fusion and expansion of the involved cortical representations. We used passive tactile finger co-activation for 40 min to investigate cortical representational changes in the human somatosensory cortex. Magnetic source imaging revealed that the euclidean distance between median and ulnar nerve somatosensory evoked fields (SEF) was significantly reduced after application of 600 synchronous airpuff stimuli to the fingertips of four fingers. In the control experiment without co-activation no significant change in distance was observed. Perception threshold and spatial two-point discrimination were not affected by the synchronous stimulation. This is in contrast to blind three-finger Braille readers who frequently mislocalize stimuli applied to the reading fingers. This points to a lack of behavioural relevance or the short duration of co-activation.     

The profile of the recovery cycle in human primary and secondary somatosensory cortex: a magnetoencephalography study.

OBJECTIVE: To estimate the lifetime of sensory memory in human primary (SI) and secondary (SII) somatosensory cortex with a view to furthering our understanding of the roles played by these cortices in the processing of tactile information. METHODS: Somatosensory evoked fields (SEFs) were recorded following trains of 5 electrical pulses applied to the right median nerve at the wrist using a whole-head 80 channel magnetoencephalography (MEG) system. Recordings were acquired for trains of pulses with differing interstimulus intervals (ISIs) occurring at 100, 200, 300, 400 and 500 ms. The profile of SEF intensities for the different ISIs provided an estimate of the recovery cycle of evoked neuronal activity, and the time constant of the exponential curve fitted to the recovery cycle was calculated to obtain a putative measure of the lifetime of somatic sensory memory in SI and SII. RESULTS: The estimated time constants were 0.11+/-0.06 s (mean+/-SD) in SI and 0.82+/-0.34 s in SII. The mean time constant in SII was significantly longer than that in SI (Student's paired t test: P=0.021; analysis of variance: F(1,3)=19.7, P=0.021). CONCLUSIONS: These data indicate that the lifetime of somatic sensory memory is of longer duration in higher order cortical areas than in primary sensory cortex in the somatosensory information processing system.     

Primary somatosensory cortex is actively involved in pain processing in human

We recorded somatosensory evoked magnetic fields (SEFs) by a whole head magnetometer to elucidate cortical receptive areas involved in pain processing, focusing on the primary somatosensory cortex (SI), following painful CO(2) laser stimulation of the dorsum of the left hand in 12 healthy human subjects. In seven subjects, three spatially segregated cortical areas (contralateral SI and bilateral second (SII) somatosensory cortices) were simultaneously activated at around 210 ms after the stimulus, suggesting parallel processing of pain information in SI and SII. Equivalent current dipole (ECD) in SI pointed anteriorly in three subjects whereas posteriorly in the remaining four. We also recorded SEFs following electric stimulation of the left median nerve at wrist in three subjects. ECD of CO(2) laser stimulation was located medial-superior to that of electric stimulation in all three subjects. In addition, by direct recording of somatosensory evoked potentials (SEPs) from peri-Rolandic cortex by subdural electrodes in an epilepsy patient, we identified a response to the laser stimulation over the contralateral SI with the peak latency of 220 ms. Its distribution was similar to, but slightly wider than, that of P25 of electric SEPs. Taken together, it is postulated that the pain impulse is received in the crown of the postcentral gyrus in human.