Influence of magnetic resonance imaging on somatosensory and brain-stem auditory evoked potentials in man

Summary There is still a need to prove that even static magnetic fields up to 1.5 T used in magnetic resonance imaging (MRI) are biologically safe and harmless for humans. Recordings of median and ulnar nerves and brain-stem auditory evoked potentials in 20 patients were completed prior to and after MRI investigation of the central nervous system. Neither the somatosensory nor the auditory evoked potentials exhibited any significant change of latencies, interpeak latencies or amplitudes. Since these electrophysiological parameters are highly dependent on the quality of nerve conduction and integrity of information processing in various nuclei, it may be assumed that MRI causes no lasting changes in either respect.     

Origin and distribution of brain-stem somatosensory evoked potentials in humans.

The distribution of somatosensory evoked potentials (SEPs) recorded from the brain-stem surface was studied to investigate their generator sources in 14 patients during surgical exploration of the posterior fossa. Two distinct SEPs of different morphologies and electrical orientation were obtained by median nerve stimulation. A small positive-large negative-late prolonged positive wave was recorded from the cuneate nucleus and its vicinity. There was a phase-reversal between the cuneate nucleus and the ventral surface of the medulla, depicting a dipole for dorso-ventral organization. From the pons and midbrain, triphasic waves with predominant negativity were obtained. This type of SEP had identical wave forms between the dorsal, lateral and ventral surface of the pons and midbrain. It showed an increase in negative peak latency as the recording sites moved rostrally, suggesting an ascending axial orientation. In a patient with pontine hemorrhage, the killed end potential, a large monophasic positive potential was obtained from the lesion. This potential occurs when an impulse approaches but never passes beyond the recording electrode. Therefore, the triphasic SEP from the pons and midbrain reflects an axonal potential generated in the medial lemniscal pathway.     

Gating of somatosensory input by human prefrontal cortex

Somatosensory evoked potentials (SEPs) to median nerve stimulation were recorded in controls and in patients with focal lesions in dorsolateral prefrontal cortex (PFCx). Unilateral PFCx lesions increased the amplitude of the P26 component generated in postcentral areas 1 and 2. The amplitudes of the N28, P45 and N67 SEP components recorded over post-rolandic and frontal electrodes were also enhanced by PFCx damage. In contrast, the N19 component generated in postcentral area 3b was unaffected by PFCx lesions. The results indicate that PFCx exerts inhibitory modulation on sensory processing that may be mediated by corticocortical PFCx-parietal connections.     

Influence of somatosensory input on motor function in patients with chronic stroke

In healthy volunteers, reduction of somatosensory input from one hand leads to rapid performance improvements in the other hand. Thus, it is possible that reduction of somatosensory input from the healthy hand can influence motor function in the paretic hand of chronic stroke patients with unilateral hand weakness. To test this hypothesis, we had 13 chronic stroke patients perform motor tasks with the paretic hand and arm during cutaneous anesthesia of the healthy hand and healthy foot in separate sessions. Performance of a finger tapping task, but not a wrist flexion task, improved significantly with anesthesia of the hand, but not the foot. This effect progressed with the duration of anesthesia and correlated with baseline motor function. We conclude that cutaneous anesthesia of the healthy hand elicits transient site-specific improvements in motor performance of the moderately paretic hand in patients with chronic stroke, consistent with interhemispheric competition models of sensorimotor processing.     

Specific somatosensory processing in somatosensory area 3b for human thumb: a neuromagnetic study.

OBJECTIVES: We examined the relation between somatosensory N20m primary responses and high-frequency oscillations (HFOs) after thumb and middle finger stimulation. METHODS: Somatosensory evoked fields (SEFs) from 12 subjects were measured following electric stimulation of the thumb and middle finger. SEFs were recorded with a wide bandpass (3-2000 Hz) and then N20m and HFOs were separated by subsequent 3-300 and 300-900 Hz bandpass filtering. RESULTS: The N20m peak-to-peak amplitude did not differ significantly between thumb and middle finger SEFs. In contrast, HFOs had a significantly larger number of peaks and were higher in the maximum amplitude and the total amplitude after thumb stimulation than after middle finger stimulation. CONCLUSIONS: Our present data demonstrate a different relation between N20m and HFOs after thumb and middle finger stimulation. In view of the fact that the human thumb has uniquely evolved functionally and morphologically, the somatosensory information from the thumb will be processed differently for a fine motor control. We speculate that HFOs are generated by inhibitory interneurons in layer 4 in area 3b. Thus, enhanced activity of interneurons reflected by high amplitude HFOs exerts stronger inhibition on downstream pyramidal cells in area 3b for thumb stimulation.     

Interactive processing of sensory input and motor output in the human hippocampus.

Recent studies of visuomotor integration suggest that the motor system may be intimately involved in the detection of salient features of the sensory scene. The final stages of sensory processing occur in hippocampal structures. We measured human neuromagnetic responses during motor reaction to an auditory cue embedded in high-speed multimodal stimulation. Our results demonstrate that large-scale cognitive networks may recruit additional resources from the hippocampus during sensorimotor integration. Hippocampal activity from 300 msec before to 200 msec after cued movements was enhanced significantly over that observed during self-paced movements. The dominant hippocampal activity appeared equally synchronized to both sensory input and motor output, consistent with timing by an intrinsic mechanism, possibly provided by ongoing theta oscillations     

Descending projections from the dysgranular zone of rat primary somatosensory cortex processing deep somatic input

In the mammalian somatic system, peripheral inputs from cutaneous and deep receptors ascend via different subcortical channels and terminate in largely separate regions of the primary somatosensory cortex (SI). How these inputs are processed in SI and then projected back to the subcortical relay centers is critical for understanding how SI may regulate somatic information processing in the subcortex. Although it is now relatively well understood how SI cutaneous areas project to the subcortical structures, little is known about the descending projections from SI areas processing deep somatic input. We examined this issue by using the rodent somatic system as a model. In rat SI, deep somatic input is processed mainly in the dysgranular zone (DSZ) enclosed by the cutaneous barrel subfields. By using biotinylated dextran amine (BDA) as anterograde tracer, we characterized the topography of corticostriatal and corticofugal projections arising in the DSZ. The DSZ projections terminate mainly in the lateral subregions of the striatum that are also known as the target of certain SI cutaneous areas. This suggests that SI processing of deep and cutaneous information may be integrated, to a certain degree, in this striatal region. By contrast, at both thalamic and prethalamic levels as far as the spinal cord, descending projections from DSZ terminate in areas largely distinguishable from those that receive input from SI cutaneous areas. These subcortical targets of DSZ include not only the sensory but also motor-related structures, suggesting that SI processing of deep input may engage in regulating somatic and motor information flow between the cortex and periphery.     

Effects of somatosensory input on central fatigue: a pilot study.

OBJECTIVE: Depression of motor evoked potentials (MEPs) following transcranial magnetic stimulation (TMS) may be a sign of central motor fatigue. As a pilot study, we have examined whether post-exercise MEP depression can be compensated by application of sensory stimuli prior to TMS. METHODS: We studied 15 healthy volunteers (aged 21-28 years) who were required to perform an exercise protocol of ankle dorsiflexion until force fell below 66% of maximum force. MEPs were recorded from the right tibialis anterior muscle. Prior to TMS, electrical stimuli were applied to the ipsilateral sural nerve with an individual interstimulus interval between 50 and 80 ms. RESULTS: MEP areas decreased after exercise. When a sensory stimulus was administered MEPs did not change. CONCLUSION: We conclude that the effects of central fatigue may be influenced by application of sensory stimuli.     

Dynamics of neuronal processing in rat somatosensory cortex.

Recently, the study of sensory cortex has focused on the context-dependent evolution of receptive fields and cortical maps over millisecond to second time-scales. This article reviews advances in our understanding of these processes in the rat primary somatosensory cortex (SI). Subthreshold input to individual rat SI neurons is extensive, spanning several vibrissae from the center of the receptive field, and arrives within 25 ms of vibrissa deflection. These large subthreshold receptive fields provide a broad substrate for rapid excitatory and inhibitory multi-vibrissa interactions. The 'whisking' behavior, an approximately 8 Hz ellipsoid movement of the vibrissae, introduces a context-dependent change in the pattern of vibrissa movement during tactile exploration. Stimulation of vibrissae over this frequency range modulates the pattern of activity in thalamic and cortical neurons, and, at the level of the cortical map, focuses the extent of the vibrissa representation relative to lower frequency stimulation (1 Hz). These findings suggest that one function of whisking is to reset cortical organization to improve tactile discrimination. Recent discoveries in primary visual cortex (VI) demonstrate parallel non-linearities in center-surround interactions in rat SI and VI, and provide a model for the rapid integration of multi-vibrissa input. The studies discussed in this article suggest that, despite its original conception as a uniquely segregated cortex, rat SI has a wide array of dynamic interactions, and that the study of this region will provide insight into the general mechanisms of cortical dynamics engaged by sensory systems.     

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.     

Contribution of different somatosensory afferent input to subcortical somatosensory evoked potentials in humans

ObjectivesTo investigate the subcortical somatosensory evoked potentials (SEPs) to electrical stimulation of either muscle or cutaneous afferents.MethodsSEPs were recorded in 6 patients suffering from Parkinson’s disease (PD) who underwent electrode implantation in the pedunculopontine (PPTg) nucleus area. We compared SEPs recorded from the scalp and from the intracranial electrode contacts to electrical stimuli applied to: 1) median nerve at the wrist, 2) abductor pollicis brevis motor point, and 3) distal phalanx of the thumb. Also the high-frequency oscillations (HFOs) were analysed.ResultsAfter median nerve and pure cutaneous (distant phalanx of the thumb) stimulation, a P1-N1 complex was recorded by the intracranial lead, while the scalp electrodes recorded the short-latency far-field responses (P14 and N18). On the contrary, motor point stimulation did not evoke any low-frequency component in the PPTg traces, nor the N18 potential on the scalp. HFOs were recorded to stimulation of all modalities by the PPTg electrode contacts.ConclusionsStimulus processing within the cuneate nucleus depends on modality, since only the cutaneous input activates the complex intranuclear network possibly generating the scalp N18 potential.SignificanceOur results shed light on the subcortical processing of the somatosensory input of different modalities.     

The influence of interfering input from the peroneal nerve on tibial-nerve somatosensory evoked potential.

Using a conditioning-test paradigm, we studied the recovery function of tibial nerve somatosensory evoked potentials (SEPs) conditioned by preceding peroneal nerve stimulation. The inter-stimulus intervals (ISIs) ranged from 0 to 400 msec, where 0 msec indicated simultaneous arrival of tibial and peroneal nerve volleys at the L1 spine. The recovery curve was W-shaped, showing two peaks of SEP suppression, maximum at 6 msec ISI (1st phase) and 50-75 ISI msec (2nd phase). In the 1st phase suppression, we found distinct differences in wave forms between 0-2 msec ISI and 4-6 msec ISI. At 0-2 msec ISI, P40-N50-P60 amplitude decreased and latencies shortened, while P31 and N35 were unchanged. At 4-6 msec ISI, all peaks, possibly excluding P31, were markedly depressed. We attribute the former change to an "occlusive effect" and the latter to an "inhibitory effect," each mediated via a central synaptic network between the two nerves. The attenuation of the 2nd but not the 1st phase suppression by peroneal nerve block distal to the stimulating electrodes provided evidence that the 2nd phase suppression resulted primarily from interfering afferent signals generated by peroneal nerve peripheral receptors, activated by foot movement.     

Habituation within the somatosensory processing hierarchy

Habituation is a basic process of learning evident in a decrement in neuronal/behavioral responses to repeated sensory stimulation. It is generally accepted that habituation affects all sensory systems in the human brain, including the somatosensory network. However, it is not clear where habituation originates within this hierarchically organized network. In this study, we examined whether habituation effects increase relatively uniformly along the processing hierarchy or rather distinctly at a particular processing stage. We addressed these questions by performing functional magnetic resonance imaging (fMRI) on 43 healthy subjects during unilateral electrical median nerve stimulation using a block design. We found a time-dependent decrease in the positive BOLD response (indicative of habituation) in all areas of the somatosensory network with the exception of Brodmann area (BA) 3b. The increase in habituation within the presumed processing stream was most pronounced between subareas of the primary somatosensory cortex (BA3b, BA1, BA2), and no further increase in habituation effects was observed in the subsequent processing stages within either the secondary somatosensory cortex or the insula. Moreover, we found a relatively strong habituation effect within the thalamus. These findings indicate that the increase in habituation along the processing hierarchy is measurable primarily between subareas of the primary somatosensory cortex, and we hypothesize that this increase originates in thalamocortical interactions early in the processing stream.     

Vestibular, somatosensory, and auditory input to the thalamus of the cat.

Responses were recorded and analyzed for 334 single units in the ventral, posterior, and intralaminar groups of thalamic nuclei of the cat. Units were tested for a response after (i) electrical stimulation of the vestibular nerve: (ii) electrical stimulation of the four paw pads and natural stimulation of joint, muscle, and cutaneous receptors of the limbs, trunk, and head (somatic stimulation); and (iii) electrical stimulation of the cochlear nerve and sound (auditory stimuli). Forty-one percent of the units responded to these stimuli. Vestibular stimulation activated 16% of the responsive units. These units were found primarily in the posterior nucleus and the border region between it and the ventral posterolateral nucleus. Seventy-three percent of vestibular-activated units also responded to at least one other modality of sensory stimuli. No evidence was found for a thalamic region where the majority of units responded at short latency to vestibular nerve stimulation. Ninety percent of the responsive units were activated by somatic stimuli. These units could be divided into two groups. One group was composed of units that were activated exclusively by somatic stimuli and had a small contralateral receptive field. These units were found primarily in the ventral posterolateral nucleus. The other group had a bilateral receptive field or was activated by more than one modality of sensory stimuli. These units were found primarily in the posterior nucleus and the border area of the ventral posterolateral nucleus. Units that responded to auditory stimulation (10% of responsive units) were found in the posterior nucleus and the medial geniculate nucleus.     

Unusual pattern of somatosensory and brain-stem auditory evoked potentials after cardio-respiratory arrest

Two patients in coma after cardio-pulmonary arrest showed bilateral absence of all brain-stem auditory evoked potentials contrasting with normal brain-stem reflexes and normal somatosensory cortical evoked potentials. In both patients pre-existing dysfunction of peripheral auditory structures could be ruled out. Subsequent neuropathological analysis showed that the anoxic-ischaemic lesions were restricted to Sommer's sector and the Purkinje cells. These unusual data suggest the hypothesis that a severe hypoxic-ischaemic insult may impair cochlear function and interfere with the activation of the intact auditory pathways.