Rapid reversible changes to multiple levels of the human somatosensory system following the cessation of repetitive contractions: a somatosensory evoked potential study.

OBJECTIVE: Numerous somatosensory evoked potential (SEP) studies have provided clear evidence that during repetitive voluntary movement, the transmission of somatosensory afferent information is attenuated. The objective of this work was to determine if this gating phenomenon could persist beyond the period of repetitive movement. METHODS: We recorded spinal, brainstem, and cortical SEPs to median nerve stimulation before and immediately after a modified 20 min repetitive typing task that did not involve the thenar muscles. RESULTS: There were significant decreases in pre-central cortical and subcortical SEP amplitudes for several minutes following task cessation. CONCLUSIONS: These results demonstrate the persistence of the gating phenomenon beyond the cessation of the actual repetitive movement. They also indicate that plastic changes do occur in cortical and subcortical components of the somatosensory system, following voluntary repetitive contractions. SIGNIFICANCE: The persistence of changes in somatosensory processing beyond the period of repetitive activity may be relevant to the initiation of overuse injuries.     

Scalp distribution of the earliest cortical somatosensory evoked potential to tibial nerve stimulation: proposal of a new recording montage.

OBJECTIVE: To investigate the most reliable method to record the earliest cortical somatosensory evoked potential (SEP) after tibial nerve stimulation. The 'gating' phenomenon was used to dissociate the overlapping cortical SEP components. METHODS: In 11 subjects we recorded the scalp SEPs at rest, during the voluntary (active gating) and passive (passive gating) foot movement and during the isometric calf muscle contraction (isometric gating). RESULTS: At the vertex the P40 amplitude was reduced in all the gating conditions. Instead, both the P40 response recorded in the parietal region ipsilateral to the stimulation (indicated as P40par) and the fronto-temporal N37 potential were reduced in amplitude only during the passive foot movement. CONCLUSIONS: The same behaviour of the N37 and P40par potentials suggests that they can represent the opposite counterparts of the same dipolar generator. Instead, the real P40 amplitude, which is affected in all the gating conditions, is recorded at the vertex and might be generated by a different source. We conclude that the montage obtained by referring a temporal electrode contralateral to the stimulation to an ipsilateral parietal lead can reliably record the earliest cortical component (N37/P40par) after tibial nerve stimulation.     

Task-relevant selective modulation of somatosensory afferent paths from the lower limb

Leg movement attenuates initial somatosensory evoked potentials (SEPS) from both cutaneous and muscle afferent origin. To date, as different sensory inputs become relevant for task performance, selective facilitation from such movement-related gating influences has not been shown. We hypothesized that initial SEP amplitudes from cutaneous (sural nerve, SN) and muscle afferent (tibial nerve, TN) sources are dependent on the relevance of the specific afferent information to task performance. SEPs were obtained at rest and during three movement conditions. In each movement condition, the left foot was passively moved episodically and additional cutaneous 'codes' of sensory information were applied to the dorsum of the left foot. Subjects were instructed to: simply relax (passive), or to make a response following the cessation of movement, dependent either on the cutaneous code (cutaneous task), or the passive movement trajectory of the left foot (position task). Passive movement, with no required subsequent response, attenuated initial TN and SN SEPs to approximately 40% of that at rest (p < 0.05). Versus passive movement, when cutaneous inputs provided the relevant cue for the task, mean SN SEPs significantly increased (p < 0.05), and when the proprioceptive inputs provided the relevant cue for the task, mean TN SEPs significantly increased (p < 0.05). We conclude that specific relevancy of sensory information selectively facilitates somatosensory paths from movement-related attenuation.     

"Gating" of human short-latency somatosensory evoked cortical responses during execution of movement. A high resolution electroencephalography study.

The present study aimed at investigating gating of median nerve somatosensory evoked cortical responses (SECRs), estimated during executed continuous complex ipsilateral and contralateral sequential finger movements. SECRs were modeled with an advanced high resolution electroencephalography technology that dramatically improved spatial details of the scalp recorded somatosensory evoked potentials. Integration with magnetic resonance brain images allowed us to localize different SECRs within cortical areas. The working hypothesis was that the gating effects were time varying and could differently influence SECRs. Maximum statistically significant (p<0. 01) time-varying gating (magnitude reduction) of the short-latency SECRs modeled in the contralateral primary motor and somatosensory and supplementary motor areas was computed during the executed ipsilateral movement. The gating effects were stronger on the modeled SECRs peaking 30-45 ms (N30-P30, N32, P45-N45) than 20-26 ms (P20-N20, P22, N26) post-stimulus. Furthermore, the modeled SECRs peaking 30 ms post-stimulus (N30-P30) were significantly increased in magnitude during the executed contralateral movement. These results may delineate a distributed cortical sensorimotor system responsible for the gating effects on SECRs. This system would be able to modulate activity of SECR generators, based on the integration of afferent somatosensory inputs from the stimulated nerve with outputs related to the movement execution.     

“Gating” of human short-latency somatosensory evoked cortical responses during execution of movement. A high resolution electroencephalography study

The present study aimed at investigating gating of median nerve somatosensory evoked cortical responses (SECRs), estimated during executed continuous complex ipsilateral and contralateral sequential finger movements. SECRs were modeled with an advanced high resolution electroencephalography technology that dramatically improved spatial details of the scalp recorded somatosensory evoked potentials. Integration with magnetic resonance brain images allowed us to localize different SECRs within cortical areas. The working hypothesis was that the gating effects were time varying and could differently influence SECRs. Maximum statistically significant (p<0.01) time-varying gating (magnitude reduction) of the short-latency SECRs modeled in the contralateral primary motor and somatosensory and supplementary motor areas was computed during the executed ipsilateral movement. The gating effects were stronger on the modeled SECRs peaking 30–45 ms (N30–P30, N32, P45–N45) than 20–26 ms (P20–N20, P22, N26) post-stimulus. Furthermore, the modeled SECRs peaking 30 ms post-stimulus (N30–P30) were significantly increased in magnitude during the executed contralateral movement. These results may delineate a distributed cortical sensorimotor system responsible for the gating effects on SECRs. This system would be able to modulate activity of SECR generators, based on the integration of afferent somatosensory inputs from the stimulated nerve with outputs related to the movement execution.     

Reduction in amplitude of the subcortical low- and high-frequency somatosensory evoked potentials during voluntary movement: an intracerebral recording study.

OBJECTIVE: To investigate whether the reduction of amplitude of the scalp somatosensory evoked potentials (SEPs) during movement (gating) is due to an attenuation of the afferent volley at subcortical level. METHODS: Median nerve SEPs were recorded from 9 patients suffering from Parkinson's disease, who underwent implant of intracerebral (IC) electrodes in the subthalamic nucleus or in the globus pallidum. SEPs were recorded from Erb's point ipsilateral to stimulation, from the scalp surface and from the IC leads, at rest and during a voluntary flexo-extension movement of the stimulated wrist. The recorded IC traces were submitted to an off-line filtering by a 300-1500 bandpass to obtain the high-frequency SEP bursts. RESULTS: IC leads recorded a triphasic component (P1-N1-P2) from 14 to 22 ms of latency. The amplitudes of the scalp N20, P20 and N30 potentials and of the IC triphasic component were significantly decreased during movement, while the peripheral N9 amplitude remained unchanged. Also the IC bursts, whose frequency was around 1000 Hz, were reduced in amplitude by the voluntary movement. CONCLUSIONS: Since the IC triphasic component is probably generated by neurons of the thalamic ventro-postero-lateral nucleus, which receive the somatosensory afferent volley, the P1-N1 amplitude reduction during movement suggests that the gating phenomenon involves also the subcortical structures.     

Generalisability of sensory gating during passive movement of the legs

Movement-related gating of somatosensory evoked potentials in the upper limb is restricted mainly to nerve stimulation supplying the moved limb segment. In the lower limb, this principle may not be followed. Tibial nerve (stimulation at the knee) somatosensory evoked potentials (SEPs) and soleus H reflexes exhibit quite similar patterns of modulation during movement. We hypothesised that movement-related gating of initial SEPs in the leg would be generalised from ipsilateral to contralateral leg movement and that such sensory gating would not be generalised to modalities with no functional relevance to the movement. Somatosensory, visual, and auditory evoked potentials (SEPs, VEPs, and AEPs) were recorded from scalp electrodes during unilateral passive movement. Short-latency tibial nerve SEPs, representing the first cortical components, and soleus H reflexes in both the moved leg and the stationary leg were attenuated compared to non-movement controls (p<0.05). Neither VEPs nor middle latency AEPs were modulated (p>0.05). We conclude that sensory gating occurs during contralateral movement. This gating is absent in other sensory modalities with no apparent functional relationship to the imposed movement.     

Specific gating of the early somatosensory evoked potentials during active movement

The gating effect of self-paced rapid flexion movements of the fingers on the early somatosensory evoked potentials following electrical stimulation of the median nerve at the wrist was studied in normal volunteers. Triggering of the median nerve stimulation by the EMG signals with a delay of 100 msec showed that the slow positive wave of the movement-associated potential was not directly responsible for the SEP amplitude variations observed. The nerve action potential at Erb's point as well as far-field components P9 and P11 were unchanged by the active movements. Far-field components P13-P14, which are presumably generated in the medial lemniscus, were not significantly modified. An enhancing effect on the widespread N18 component was found, which is in favour of a subcortical gating process. The parietal component N20 was unchanged by active movement interference whereas the frontal P22 component showed a marked suppression. A fronto-parietal dissociation was thus disclosed which could be in favour of separate cortical generators in the debate on the origin of SEP components. An important gating effect was observed on parietal P27 and frontal N30 components, the latter being considerably reduced in amplitude. The parietal P45 component showed no significant alteration. Each component of the early SEPs was thus distinctly influenced by the gating process during active movement interference.     

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.     

Proprioceptive modulation of somatosensory evoked potentials during active or passive finger movements in man.

The effects of active and passive finger movements on somatosensory potentials evoked by stimulation of the median nerve at the wrist or of finger I were investigated in 15 healthy volunteers. As compared to the resting condition, both active and passive movements of the stimulated hand fingers induced a marked reduction in the amplitude of the primary cerebral response (N20-P25 complex) as well as of the N17 SEP component, which is supposed to reflect the activity of the thalamo-cortical radiation. The following cerebral SEP components, within 100 ms after the stimulus, were also depressed during motor activity. Neither N11 nor N13 components of the cervical response, reflecting the activation of dorsal columns and dorsal column nuclei respectively, were modified. The SEP changes induced by active or passive movements were absent after ischaemic block of large group I afferent fibers from the hand, thus suggesting the relevance of the feedback generated by such peripheral afferents during movement. The results indicate that the activation of peripheral receptors (probably muscle spindle endings) during both active and passive finger movement would induce a gating effect at both cortical and subcortical (thalamic) level, which might modulate selectively the different sensory inputs to the cortex.     

Electrical somatosensory stimulation modulates hand motor function in healthy humans

In healthy people, electrical somatosensory stimulation modulates excitability in contralateral cortical motor areas. The question whether this is associated with a change in motor performance is still under debate. The effect of electrical somatosensory stimulation on motor performance of the hand was investigated in 14 healthy right-handed subjects. Subjects performed index finger and hand tapping movements as well as reach-to-grasp movements towards small and large cubes with each hand prior to (baseline condition) and following 2-hour electrical somatosensory stimulation (trains of 5 pulses at 10 Hz with 1 ms duration delivered at 1 Hz with an intensity on average 60 % above the individual somatosensory threshold) of the (i) right median nerve, (ii) left median nerve, (iii) right tibial nerve (control stimulation) and (iv) left tibial nerve (control stimulation) on separate occasions at least one week apart. The order of sessions was counterbalanced across subjects. Somatosensory stimulation of the median nerves, but not of the tibial nerves, reduced the frequency and velocity of index finger and hand tapping movements performed with the stimulated hand, compared to baseline. In contrast, the kinematics of reach-to-grasp movements remained unaffected by somatosensory stimulation. The data suggest that somatosensory stimulation interferes with the processing of highly automated open-loop motor output at the stimulated limb, as reflected by tapping movements, but not with the processing of closed-loop motor performance, as reflected by reach-to-grasp movements.     

Activation of human SII cortex during exploratory finger movement and hand clenching tasks

We used electric median nerve stimuli to elucidate the functional properties of neurons in the human secondary somatosensory cortex during exploration of small objects and muscle contraction. Somatosensory evoked fields were recorded from nine healthy subjects with a 204-channel neuromagnetometer. Electrical stimuli were applied once every 3 s to the left median nerve at the wrist. The conditions during the stimulation were rest (control session), exploration of small objects (exploration session) and clenching the hand while the wrist was being electrically stimulated (clench session). The strengths of equivalent current dipoles of evoked fields from the secondary somatosensory cortex were increased during the exploration session, but those of evoked fields were decreased by the clench session.     

Rapid cortical reorganisation and improved sensitivity of the hand following cutaneous anaesthesia of the forearm

The cortical representation of various body parts constantly changes based on the pattern of afferent nerve impulses. As peripheral nerve injury results in a cortical and subcortical reorganisation this has been suggested as one explanation for the poor clinical outcome seen after peripheral nerve repair in humans. Cutaneous anaesthesia of the forearm in healthy subjects and in patients with nerve injuries results in rapid improvement of hand sensitivity. The mechanism behind the improvement is probably based on a rapid cortical and subcortical reorganisation. The aim of this work was to study cortical changes following temporary cutaneous forearm anaesthesia. Ten healthy volunteers participated in the study. Twenty grams of a local anaesthetic cream (EMLA^®) was applied to the volar aspect of the right forearm. Functional magnetic resonance imaging was performed during sensory stimulation of all fingers of the right hand before and during cutaneous forearm anaesthesia. Sensitivity was also clinically assessed before and during forearm anaesthesia. A group analysis of functional magnetic resonance image data showed that, during anaesthesia, the hand area in the contralateral primary somatosensory cortex expanded cranially over the anaesthetised forearm area. Clinically right hand sensitivity in the volunteers improved during forearm anaesthesia. No significant changes were seen in the left hand. The clinically improved hand sensitivity following forearm anaesthesia is probably based on a rapid expansion of the hand area in the primary somatosensory cortex which presumably results in more nerve cells being made available for the hand in the primary somatosensory cortex.     

Somatosensory evoked potentials after median and tibial nerve stimulation in healthy newborns.

Cortical and spinal somatosensory evoked potentials (SEPs) have been recorded after median and tibial nerve stimulation in healthy newborns. Spinal SEPs were readily obtained and recorded in all but one neonates after stimulation of both nerves. Cortical SEPs were more frequently recorded after median nerve (87%) than after tibial nerve stimulation (73%) but the shape of cortical SEPs obtained after tibial nerve stimulation was less variable. The mean feature of cortical SEPs was a negative wave (N27) for median nerve and a positive wave (P32) for tibial nerve. The present results demonstrate the feasibility of obtaining in the same baby, spinal and cortical SEPs after stimulation of median and tibial nerve, giving information on the functional integrity of central and peripheral somatosensory pathways which supply upper and lower limbs.     

The effects of sleep on median nerve short latency somatosensory evoked potentials

The effects of sleep on median nerve short latency somatosensory evoked potentials were studied in 7 subjects made up of 6 patients being evaluated for seizure disorders by all-night electroencephalograms and 1 normal healthy volunteer. The median nerve was stimulated at the wrist, and the peripheral (N9), subcortical (P13) and early cortical (N1, P2) evoked potentials were recorded during full wakefulness and natural night-time sleep. Sleep-wake state was monitored by the simultaneously obtained polysomnogram. The latencies of the cortical responses were prolonged during non-rapid eye movement (NREM) sleep. In 3 of the subjects P2 was consistently bifid during NREM sleep only. The second component of the bifid potential, 3-4 msec longer in latency than the first, appeared to be selectively enhanced during NREM sleep whereas the first component tended to become less prominent or even disappear. This suggests that the 2 peaks have different generators that are affected differently by NREM sleep. These are clinically relevant findings for interpretation of routine clinical studies.     

The gain of initial somatosensory evoked potentials alters with practice of an accurate motor task

The gain of somatosensory afferent paths from the lower limb to the cerebral cortex was investigated during the acquisition of one target location during plantar flexion. Sensory gain was measured as the magnitude of somatosensory evoked potentials (SEPs) following electrical stimulation of a peripheral nerve in the lower limb, and was recorded from the scalp. We hypothesized gain attenuation of SEPs from sensory paths serving the limb segment responsible for target acquisition. SEP gain was studied as subjects plantar flexed about the anide to a target that was 15° beyond the occurrence of a cutaneous stimulus (cue) to the lateral border of the foot. The ‘cue’ was either fixed in one location or could appear at one of three positions in space. SEP gain was tested during practice and with task acquisition. Electroencephalographic (EEG) recordings were made of primary and secondary complexes of cortical SEPs from sural and tibial nerve stimulation, with 30–40 samples averaged per subject-condition. Electromyographic (EMG) records were made of soleus muscle H-reflexes and M-waves. Target acquisition was recorded as percent correct hits. The results showed significant attenuation in sural and tibial nerve primary SEPs with task acquisition when the cue was fixed or varied in movement space (P<0.05). Secondary SEPs from tibial nerve followed this pattern. Spinal H-reflexes only attenuated with movement per se. We conclude that the CNS preferentially reduces the cerebral inflow of sensory information once such a motor task has been successfully acquired.     

Cortical activation in area 3b related to finger movement: an MEG study

To evaluate cortical activation reflecting sensory feedback after finger movement, we recorded movement-related cerebral fields (MRCFs) following voluntary finger movement and somatosensory evoked fields for mixed (median) and pure cutaneous (radial) nerve stimulations (mSEFs and rSEFs) in six normal subjects. Equivalent current dipoles for movement-evoked field 1 (MEF1) in MRCFs and the component (70m) obtained in mSEFs, not clearly in rSEFs, were similarly distributed in each subject. They were located in area 3b, but both mean locations were significantly (p < 0.01) medial to N20m in mSEFs. MEF1 and 70m reflect similar cortical activities related to finger movement and have the same neuronal generator in area 3b, which is different from that of N20m.     

Abnormal primary somatosensory function in unilateral polymicrogyria: an MEG study

The purpose of this study is to investigate the primary somatosensory function in patients with unilateral polymicrogyria. Somatosensory evoked fields (SEFs) due to median and posterior tibial nerve stimulation were compared in the normal and dysplastic cortices of five patients with unilateral polymicrogyria. SEFs were observed in all five normal hemispheres and three dysplastic hemispheres. Latencies of N20m and P38m, the first cortical components of and SEFs for median nerve and tibial nerve stimulation, were all within the normal range in both normal and dysplastic hemispheres. The amplitudes of the N20m and P38m in the dysplastic hemispheres were smaller in one patient and larger in two patients compared to the normal hemispheres. Equivalent current dipoles of N20m and P38m were localized on the anatomical central sulcus of the normal hemispheres and over the central area of the dysplastic hemispheres. P38m dipoles were localized medial and upward to the N20m dipole in both normal and dysplastic hemispheres. N20m dipole orientation was normal in all normal hemispheres and in one dysplastic hemisphere, but abnormally inferior in two dysplastic hemispheres. P38m dipole had normal medial orientation in all hemispheres except one dysplastic hemisphere. Abnormality of the primary somatosensory function in the dysplastic cortex of patients with unilateral polymicrogyria was clearly demonstrated by magnetoencephalography with high resolution in time and space. The normal somatotopic arrangement was preserved.     

Movement gating of beta/gamma oscillations involved in the N30 somatosensory evoked potential

Evoked potential modulation allows the study of dynamic brain processing. The mechanism of movement gating of the frontal N30 component of somatosensory evoked potentials (SEP) produced by the stimulation of the median nerve at wrist remains to be elucidated. At rest, a power enhancement and a significant phase-locking of the electroencephalographic (EEG) oscillation in the beta/gamma range (25-35 Hz) are related to the emergence of the N30. The latter was also perfectly identified in presence of pure phase-locking situation. Here, we investigated the contribution of these rhythmic activities to the specific gating of the N30 component during movement. We demonstrated that concomitant execution of finger movement of the stimulated hand impinges such temporal concentration of the ongoing beta/gamma EEG oscillations and abolishes the N30 component throughout their large topographical extent on the scalp. This also proves that the phase-locking phenomenon is one of the main actors for the N30 generation. These findings could be explained by the involvement of neuronal populations of the sensorimotor cortex and other related areas, which are unable to respond to the phasic sensory activation and to phase-lock their firing discharges to the external sensory input during the movement. This new insight into the contribution of phase-locked oscillation in the emergence of the N30 and in its gating behavior calls for a reappraisal of fundamental and clinical interpretation of the frontal N30 component.     

Gating of sensory input at spinal and cortical levels during preparation and execution of voluntary movement

All bodily movements stimulate peripheral receptors that activate neurons in the brain and spinal cord through afferent feedback. How these reafferent signals are processed within the CNS during movement is a key question in motor control. We investigated cutaneous sensory-evoked potentials in the spinal cord, primary somatosensory and motor cortex, and premotor cortex in monkeys performing an instructed delay task. Afferent inputs from cutaneous receptors were suppressed at several levels in a task-dependent manner. We found two types of suppression. First, suppression during active limb movement was observed in the spinal cord and all three cortical areas. This suppression was induced by both bottom-up and top-down gating mechanisms. Second, during preparation for upcoming movement, evoked responses were suppressed exclusively in the motor cortical areas and the magnitude of suppression was correlated with the reaction time of the subsequent movement. This suppression could be induced by a top-down gating mechanism to facilitate the preparation and execution of upcoming movement.