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 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.     

Direct recording of somatosensory evoked potentials in the vicinity of the dorsal column nuclei in man: their generator mechanisms and contribution to the scalp far-field potentials

Somatosensory evoked potentials (SEPs) in the vicinity of the dorsal column nuclei in response to electrical stimulation of the median nerve (MN) and posterior tibial nerve (PTN) were studied by analyzing the wave forms, topographical distribution, effects of higher rates of stimulation and correlation with components of the scalp-recorded SEPs. Recordings were done on 4 patients with spasmodic torticollis during neurosurgical operations for microvascular decompression of the eleventh nerve. The dorsal column SEPs to MN stimulation (MN-SEPs) were characterized by a major negative wave (N1; 13 msec in mean latency), preceded by a small positivity (P1) and followed by a large positive wave (P2). Similar wave forms (P1′-N1′-P2′) were obtained with stimulation of PTN (PTN-SEPs), with a mean latency of N1′ being 28 msec. Maximal potentials of MN-SEPs and PTN-SEPs were located in the vicinity of the ipsilateral cuneate and gracile nuclei, respectively, at a level slightly caudal to the nuclei. The latencies of P1 and N1 increased progressively at more rostral cervical cord segments and medulla, but that of P2 did not. A higher rate of stimulation (16 Hz) caused no effects on P1 and N1, while it markedly attenuated the P2 component. These findings suggest that P1 and N1 of MN-SEPs, as well as P1′ and N1′ of PTN-SEPs, are generated by the dorsal column fibers, and P2 and P2′ are possibly of postsynaptic origin in the respective dorsal column nuclei.The peak latency of N1 recorded on the cuneate nucleus was identical with the scalp-recorded far-field potential of P13–14 in all patients, while no scalp components were found which corresponded to P2. These findings support the previous assumption that the scalp-recorded P13–14 is generated by the presynaptic activities of the dorsal column fibers at their terminals in the cuneate nucleus.     

Neural generators of the somatosensory evoked potentials: Recording from the cuneate nucleus in man and monkeys

The neural generators of the somatosensory evoked potentials (SEPs) elicited by electrical stimulation of the median nerve were studied in man and in rhesus monkeys. Recordings from the cuneate nucleus were compared to the far-field potentials recorded from electrodes placed on the scalp. It was found that the shape of the response from the surface of the human cuneate nucleus to stimulation of the median nerve is similar to that of the response recorded more caudally in the dorsal column, i.e., an initially small positivity followed by a negative wave that is in turn followed by a slow positive wave. The beginning of the negative wave coincides in time with the N14 peak in the SEP recorded from the scalp, and its latency is 13 msec. The response from the cuneate nucleus in the rhesus monkey has a similar shape and its negative peak appears with the same latency as the positive peak in the vertex response that has a latency of 4.5 msec; the peak negativity has a latency of about 6 msec and thus coincides with P6.2 in the vertex recording. Depth recordings from the cuneate nucleus and antidromic stimulation of the dorsal column fibers in the monkey provide evidence that the early components of the response from the surface of the cuneate nucleus are generated by the dorsal column fibers that terminate in the nucleus.The results support the hypothesis that the P14 peak in the human SEP is generated by the termination of the dorsal column fibers and that the cuneate nucleus itself contributes little to the far-field potentials.     

Discrepancy between SEPs directly recorded from the dorsal column nuclei following upper and lower limb stimulation in patients with syringomyelia

Somatosensory evoked potentials (SEPs) in response to electrical stimulation of the median nerve (MN) and posterior tibial nerve (PTN) were studied in 2 patients with syringomyelia. Intraoperative recordings were made from the surface of the dorsal column nuclei as well as from the scalp. Following MN stimulation, there was a preservation of scalp-recorded P9, P11, P13 and N20, however, there was an absence of spinal N13-P13. The dorsal column SEPs to MN stimulation were normal, characterized by a major negativity (N1), preceded by a small positivity (P1) and followed by a large positivity (P2). On the other hand, there was little or no cortical response (P37) to PTN stimulation. The dorsal column SEPs to PTN stimulation showed a disappearance of the normal P1′-N1′-P2′ configuration, being replaced by a series of small spiky waves. The syringomyelic cavity may have thus compressed the gracile dorsal column which courses more medially than the cuneate pathway, causing desynchronization of the dorsal column SEPs. These findings suggest that dorsal column pathway arising from the lower limb is more vulnerable than that from the upper limb when a cervical syrinx is present.     

Effect of manipulation and fractionated finger movements on subcortical sensory activity in man

Previous studies have shown that the somatosensory evoked potentials (SEPs) recorded from the scalp are modified or gated during motor activity in man. Animal studies show corticospinal tract terminals in afferent relays, viz. dorsal horn of spinal cord, dorsal column nuclei and thalamus. Is the attenuation of the SEP during movement the result of gating in subcortical nuclei? This study has investigated the effect of manipulation and fractionated finger movements of the hand on the subcortically generated short latency SEPs in 9 healthy subjects. Left median nerve SEPs were recorded with electrodes optimally placed to record subcortical activity with the least degree of contamination. There was no statistically significant change in amplitude or latency of the P9, N11, N13, P14, N18 and N20 potentials during rest or voluntary movement of the fingers of the left hand or manipulation of objects placed in the hand. The shape of the N13 wave form was not modified during these 3 conditions. It is concluded that in man attenuation of cortical waves during manipulation is not due to an effect of gating in the subcortical sensory relay nuclei.     

Median nerve somatosensory evoked potentials in profound hypothermia for ascending aorta repair

Median nerve somatosensory evoked potentials (SEPs) were recorded in 9 patients undergoing profound hypothermia for surgical repair of the aortic arch. In addition to the known increase in peak latencies, hypothermia gave rise to the appearance of peaks (‘P13,’ ‘N14’) inconsistently recognized at normothermia; moreover, profound hypothermia is associated with the disappearance of cortical activities around 20°, of subcortical waves at lower temperatures. The practical implications of the results are 3-fold: firstly, they suggest that the ‘P13’ and P14 should both be intracranially generated, at a pre- and postsynaptic level with respect to the cuneate nucleus, respectively; secondly, they show that some discrepancies between previous papers dealing with SEPs and hypothermia can be explained by differences in the choice of the reference; thirdly, they bring some suggestions on a better use of SEPs to monitor patients undergoing aortic arch surgery.     

Brain-stem somatosensory dysfunction in a case of long-standing left hemispherectomy with removal of the left thalamus: a nasopharyngeal and scalp SEP study

We have studied median nerve somatosensory evoked potentials (SEPs) in a patient who had undergone early surgical removal of the left cerebral hemisphere and left thalamus. Stimulation of the right side evoked normal latency P9, P11 and P13 potentials at scalp as well as at nasopharyngeal (NP) leads, while P14 and N18 potentials were absent. These SEP abnormalities, that have been described previously in cervico-medullary lesions and in comatose patients with upper brain-stem involvement, suggest that in our patient the removal of the left thalamus has caused retrograde degeneration of the cuneate-thalamic projections. Moreover, this study confirms that P13 and P14 potentials have different generators.     

Click-evoked responses from the cochlear nucleus: a study in human

Recordings from the vicinity of the cochlear nucleus in 9 patients undergoing microvascular decompression operations to relieve hemifacial spasm, trigeminal neuralgia, tinnitus, and disabling positional vertigo were conducted by placing a monopolar electrode in the lateral recess of the fourth ventricle (through the foramen of Luschka), the floor of which is the dorsolateral surface of the dorsal cochlear nucleus. The click-evoked potentials recorded by such an electrode display a slow negative wave with a peak latency of about 6–7 msec on which several sharp peaks are superimposed. None of the peaks in the recordings from the vicinity of the cochlear nucleus coincided with any vertex-positive peaks of the brain-stem auditory evoked potentials. In recordings from the lateral aspect of the floor of the fourth ventricle near the cochlear nucleus 1 patient showed 2 positive peaks, the earliest of which had a latency close to that of peak II and the second of which had a latency close to the negative peak between peaks III and IV of the brain-stem auditory evoked potentials. There is a distinct negative peak in the responses recorded from the midline of the floor of the fourth ventricle, the latency of which is only slightly shorter than that of peak V of the brain-stem auditory evoked potentials, supporting earlier findings that the sharp tip of peak V of the brain-stem auditory evoked potentials is generated by the termination of the lateral lemniscus in the inferior colliculus.     

Somatosensory evoked potentials from the thalamic sensory relay nucleus (VPL) in humans: correlations with short latency somatosensory evoked potentials recorded at the scalp

Somatosensory evoked potentials (SEPs) were recorded in humans from an electrode array which was implanted so that at least two electrodes were placed within the nucleus ventralis posterolateralis (VPL) of the thalamus and/or the medial lemniscus (ML) of the midbrain for therapeutic purposes. Several brief positive deflections (e.g., P11, P13, P14, P15, P16) followed by a slow negative component were recorded from the VPL. The sources of these components were differentiated on the basis of their latency, spatial gradient, and correlation with the sensory experience induced by the stimulation of each recording site. The results indicated that SEPs recorded from the VPL included activity volume-conducted from below the ML (P11), activity in ML fibers running through and terminating within the VPL (P13 and P14), activity in thalamocortical radiations originating in and running througn the VPL (P15, P16 and following positive components) and postsynaptic local activity (the negative component). The sources of the scalp-recorded SEPs were also analyzed on the basis of the timing and spatial gradients of these components. The results suggested that the scalp P11 was a potential volume-conducted from below the ML, the scalp P13 and P14 were potentials reflecting the activity of ML fibers, the small notches on the ascending slope on N16 may potentially reflect the activity of thalamocortical radiations, and N16 may reflect the sum of local postsynaptic activity occurring in broad areas of the brain-stem and thalamus.     

Nasopharyngeal recordings of somatosensory evoked potentials document the medullary origin of the N18 far-field

Because the nasopharyngeal electrode provides non-invasive access to the ventral brain-stem at the medullo-pontine level we used it for recording somatosensory evoked potentials (SEPs) to median nerve stimulation (non-cephalic reference). After the P9 and P11 far-fields, the nasopharyngeal SEPs disclosed a negative-going component which was interpreted as the near-field equivalent of the P14 scalp far-field generated in the caudal part of the medial lemniscus. Nasopharyngeal SEPs also revealed a large N18 with voltage and features strikingly similar to those of the scalp-recorded N18 far-field. These results suggest that N18 is generated in the medulla and not more rostrally in the brain-stem. The use of a nasopharyngeal electrode as reference for topographic brain mapping is discussed. The paper documents the feasibility and relevance of nasopharyngeal recordings for non-invasive analysis of short-latency SEPs.     

Neurophysiological evaluation of central-peripheral sensory and motor pudendal fibres

Extensive neurophysiological investigations were carried out in 18 healthy volunteer subjects, and 6 patients with neurological disease. The tests consisted of spinal and scalp somatosensory evoked potentials (SEPs) to stimulation of the dorsal nerve of penis/clitoris, motor evoked potentials (MEPs) from the bulbocavernosus muscle (BC) and anal sphincter (AS) in response to scalp and sacral root stimulation, and measurement of sacral reflex latency (SRL) from BC and AS.In the control subjects, the mean sensory total conduction time (sensory TCT), as measured at the peak of the scalp P40 wave was 40.9 msec (range: 37.8–44.2). The mean sensory central conduction time (sensory CCT = spine-to-scalp conduction time) was 27.0 msec (range: 23.5–30.4).Transcranial brain stimulation was performed by using a magnetic stimulator both at rest and during voluntary contraction of the examined muscle. Sacral root stimulation was performed at rest. Motor total conduction times (motor TCT) to BC and AS muscles were respectively 28.8 and 30.0 msec at rest, and 22.5 and 22.8 msec during contraction. Motor central conduction times (motor CCT) to sacral cord segments controlling BC and AS muscles were respectively 22.4 and 21.2 msec at rest, and 15.1 and 12.4 msec during contraction.The mean latencies of SRL were respectively 31.4 msec in the bulbocavernosus muscle and 35.9 msec in the anal sphincter. Combined or isolated abnormalities of SEPs, MEPs and SRL were found in a small group of patients with neurological disorders primarily or secondarily affecting the genito-urinary tract.     

Short-latency somatosensory evoked potentials following median nerve stimulation in Down's syndrome

Short-latency somatosensory evoked potentials (SEPs) following median nerve stimulation were recorded in 42 patients with Down's syndrome and in 42 age- and sex-matched normal subjects. There were no significant differences between the 2 groups in the absolute peak latencies of N9, N11 and N13 components. However, interpeak latencies, N9-N11, N11-N13 and N9-N13, were prolonged significantly in Down's syndrome. These findings suggest impaired impulse conduction in the proximal part of the brachial plexus, posterior roots and/or posterior column-medial lemniscal pathway. Interpeak latency N13-N20, representing conduction time from cervical cord to sensory cortex, was not significantly different between the 2 groups. Cortical potentials N20 and P25 in the parietal area and P20 and N25 in the frontal area were of significantly larger amplitude in Down's syndrome. P25 had double peaks in 16 of 42 normal subjects, but these were not apparent in any of the patients.     

Normal temporal variability of the P100

Determination of clinically significant temporal changes in P100 latency requires knowledge of the degree of normal intraindividual variability. Checkerboard visual evoked potentials using 3 check sizes (17′, 35′ and 70′) were performed serially on 20 healthy volunteers. Each subject was tested at least twice an average of 6 months apart. The P100 latency was measured at Oz with a forehead reference (Pz, O1 and O2 channels were also recorded). The overall average P100 latency change between studies for all check sizes and both eyes was 2.9 msec. However, the maximum absolute latency change was 11 msec. There was no significant difference between the average latency change for the 3 check sizes. The P100 interocular difference changed a mean of 2.5 msec (maximum 9 msec). Amplitude was more variable, with a mean change of about 1.5 μV or 25% (maximum was a 60% decrease in amplitude). A P100 latency change of up to at least 11 msec needs to be acknowledged as normal when assessing the clinical significance of changes in P100 latencies in patients. Also, P100 latency changes greater than 11 or 12 msec are very suggestive of an abnormality in the visual pathway.     

Two distinct cervical N13 potentials are evoked by ulnar nerve stimulation

To investigate the dual nature of the posterior neck N13 potential, we attempted to establish the presence of a latency dissociation between caudal (cN13) and rostral (rN13) potentials on stimulating the ulnar nerve, in view of its lower radicular entry compared to the median nerve. SEPs were evaluated in 24 normal subjects after both median and ulnar nerve stimulation. cN13 was prominent in the lower cervical segments, and rN13 was localized mainly in the upper ones using anteroposterior and longitudinal bipolar montage, respectively. The N9-cN13 interpeak latency did not differ significantly from N9-rN13 when stimulating the median nerve. On the other hand, the N9-rN13 interpeak was significantly longer than the N9-cN13 interpeak when the ulnar nerve was stimulated. The rN13 presented the same latency as P13-P14 far-field potentials in 17 out of 24 ulnar nerves tested. Therefore, the ulnar nerve stimulation evokes two distinct posterior neck N13 potentials. It is widely accepted that the caudal N13 is a postsynaptic potential reflecting the activity of the dorsal horn interneurons in the lower cervical cord. We suggest that the rostral N13 is probably generated close to the cuneate nucleus, which partly contributes to the genesis of P13-P14 far-field potentials.     

Scalp-recorded short and middle latency peroneal somatosensory evoked potentials in normals: comparison with peroneal and median nerve SEPs in patients with unilateral hemispheric lesions

Peroneal somatosensory evoked potentials (SEPs) were performed on 23 normal subjects and 9 selected patients with unilateral hemispheric lesions involving somatosensory pathways.Recording obtained from right and left peroneal nerve (PN) stimulations were compared in all subjects, using open and restricted frequency bandpass filters. Restricted filter (100–3000 Hz) and linked ear reference (A1–A2) enhanced the detection of short latency potentials (P1, P2, N1 with mean peak latency of 17.72, 21.07, 24.09) recorded from scalp electrodes over primary sensory cortex regions. Patients with lesions in the parietal cortex and adjacent subcortical areas demonstrated low amplitude and poorly formed short latency peroneal potentials, and absence of components beyond P3 peak with mean latency of 28.06 msec. In these patients, recordings to right and left median nerve (MN) stimulation showed absence or distorted components subsequent to N1 (N18) potential.These observations suggest that components subsequent to P3 potential in response to PN stimulation, and subsequent to N18 potential in response to MN stimulation, are generated in the parietal cortical regions.     

Intracranial recording from the brain-stem and the trigeminal nerve following upper lip stimulation

Short latency evoked potentials following stimulation of the upper lip were recorded intracranially during neurosurgical procedures in 14 patients. In 10 patients, a suboccipital craniectomy provided direct access to the trigeminal root and the pons at the root entry zone. Direct recordings from the trigeminal root were characterized by a large triphasic potential at 2.4–2.7 msec. The latency of this potential increased as a result of moving the recording electrode proximally towards the brain-stem. The same potential could be recorded from the brain-stem surface at a latency suggesting an intra-axial presynaptic origin. A second component, N4.7, was recorded from over the most rostral aspect of the brain-stem in 3 patients and from the tentorium free edge in 4 patients. This potential of smaller amplitude did not show significant difference in latency or polarity at various electrode locations, suggesting a deep diencephalic origin remote from the recording electrode.     

Comparison in man of short latency averaged evoked potentials recorded in thalamic and scalp hand zones of representation

Recordings were performed in the thalamus of 13 patients suffering from either abnormal movements or intractable pain, with the aim of delimiting the region to be destroyed or stimulated in order to diminish the syndrome. In 11 of these patients averaged evoked potentials were recorded simultaneously from the scalp and specific thalamus (VP) hand area levels following median nerve stimulation. These recordings were done during the operation or afterwards when an electrode was left in place for a program of stimulation.The latencies of onsets and peaks on the scalp ‘P15’ were compared with those of the VP wave; a clear correspondence was found. Moreover, when increased stimulation was used, both waves began to develop in parallel. Thus in the contralateral ‘P15’ a component exists due to the field produced by the thalamic response. To explain the presence of an ipsilateral scalp ‘P15’ wave, we propose that a second wave having the same latency and a slightly shorter peak exists on the scalp due to a field produced by a brain-stem response. This double origin of ‘P15’ is also shown by the different changes which the ipsilateral and contralateral waves present during changes in alertness.The scalp ‘N18–N20’ is also composed of at least 2 components. The first peak appears on the scalp with a latency shorter than that of the negativity which develops in the thalamus. The N wave, moreover, increases in latency with rapid stimulus repetition. We propose with others that ‘N18’ is a cortical event reflecting the arrival of the thalamo-cortical volley. The second component, ‘N20,’ has a peak latency closely correlated to that of the thalamic negativity. This component was present alone in ‘N’ when rapid stimulation (> 4/sec) was used, which did not change the thalamic response. It must be a field produced by the thalamic negativity.     

Interactions of somatosensory evoked potentials: simultaneous stimulation of two nerves

To analyse the mechanism by which sensory inputs are integrated, interactions of somatosensory evoked potentials (SEPs) in response to simultaneous stimulation of two nerves were examined in 12 healthy subjects. Right, left and bilateral median nerves were stimulated in random order so that a precise comparison could be made among the SEPs. The arithmetical sum of the independent right and left median nerve SEPs was almost equal within 40 msec of stimulus onset to that evoked by the simultaneous stimulation of bilateral median nerves. However, a difference emerged after 40 msec. The greatest difference was recorded after 100 msec. Sensory information from right and left median nerves may interact in the late phase of sensory processing. Left median, left ulnar, and both nerves together were stimulated. The sum of the SEPs of left median and ulnar nerves was not equal to that evoked by the simultaneous stimulation of the two nerves even at early latencies. Differences between them were first recorded at 14–18 msec and became greater after 30–40 msec. It is suggested that the neural interactions between impulses in the median and ulnar nerves begin below the thalamic level.     

A prospective 1 year follow-up study with somatosensory potentials evoked by stimulation of the posterior tibial nerve in patients with supratentorial cerebral infarction

Somatosensory potentials evoked by stimulation of the posterior tibial nerve (tibial nerve SEPs) were studied in 40 patients with supratentorial non-haemorrhagic cerebral infarction and in 25 control subjects. SEPs were recorded twice in 39 patients and thrice in 35 patients. The first examination was carried out 4–19 days after the onset of the symptoms, the second examination 56–100 days after the stroke, and the third examination 348–393 days after the stroke. Increased side-to-side differences in the P57 and N75 peak latencies and absence of the P40 peak were the most frequent abnormal findings. The latency abnormalities were associated with involvement of the subcortical white matter of the rolandic region. The absence of the P40 peak was, in contrast, closely related to the extension of the infarcted area into the cortical gray matter of during the acute stage, 51% of patients had abnormal SEPs in the second examination and 43% of patients in the third examination. A nearly significant decrease was observed in the number of latency abnormalities, but the number of amplitude abnormalities, including absent responses, did not change during the 1 year follow-up period.     

Pain-related somatosensory evoked potentials following CO2 laser stimulation of foot in man

Since our previous study of pain somatosensory evoked potentials (SEPs) following CO₂ laser stimulation of the hand dorsum could not clarify whether the early cortical component NI was generated from the primary somatosensory cortex (SI) or the secondary somatosensory cortex (SII) or both, the scalp topography of SEPs following CO₂ laser stimulation of the foot dorsum was studied in 10 normal subjects and was compared with that of the hand pain SEPs and the conventional SEPs following electrical stimulation of the posterior tibial nerve recorded in 8 and 6 of the 10 subjects, respectively. Three components (N1, N2 and P2) were recorded for both foot and hand pain SEPs. N1 of the foot pain SEPs was maximal at the midline electrodes (Cz or CPz) in all data where that potential was recognized, but the potential field distribution was variable among subjects and even between two sides within the same subject. N1 of the hand pain SEPs was maximal at the contralateral central or midtemporal electrode. The scalp distribution of N2 and P2, however, was not different between the foot and hand pain SEPs. The mean peak latency of N1 following stimulation of foot and hand was found to be 191 msec and 150 msec, respectively, but there was no significant difference in the interpeak latency of Nl-N2 between foot and hand stimulation. It is therefore concluded that NI of the foot pain SEPs is generated mainly from the foot area of SI. The variable scalp distribution of the N7 component of the foot pain SEPs is likely due to an anatomical variability among subjects and even between sides.