The human cervical and lumbo-sacral evoked electrospinogram. Data from intra-operative spinal cord surface recordings.

We have undertaken the analysis of the human 'evoked electrospinogram' during intra-dural surgical explorations in 20 patients. Averaged spinal cord surface evoked potentials to peripheral nerve electrical stimulation were obtained from various restricted loci on the pial surface of the cervical and lumbo-sacral spinal cord. The brachial plexus P9 potential and its lumbo-sacral counterpart P17 were recorded as ubiquitous initial far-field positivities. The pre-synaptic compound action potentials N11 and N21 dwelt on the ascending slope of N13 and N24 respectively. They were composed of 1-5 sharp peaks and collected from the dorsal and dorso-lateral positions mainly, on the cervical and lumbo-sacral cord respectively. They are thought to be generated in the proximal portion of the dorsal root, the dorsal funiculus and the afferent collaterals to the dorsal horn. Compound action potentials could also be gathered from the surface of the dorsal roots, the cervical N10 and lumbo-sacral N19 potentials. The large cervical N13 and lumbo-sacral N24 waves originate from a dorso-ventral post-synaptic dipole, generated in deep laminae of the dorsal horn during the activation of large diameter afferent fibers. These waves were maximal on the main entry cord segments of the stimulated nerves and fell off on the 1-4 more rostral and caudal segments. The N2 wave is the dorsal component of another post-synaptic dorso-ventral dipole generated in deep laminae of the dorsal horn but activated by medium diameter afferent fibers. The latest event was the N3 wave, also possibly part of a dorso-ventral post-synaptic dipole, and generated by cells in the dorsalmost and deep dorsal horn laminae during the activation of small diameter afferent fibers. The P wave was a prolonged positive deflection which carried the N2 and N3 waves. It is the manifestation of pre-synaptic inhibition on primary afferent fibers. A supra-segmental ascending spinal cord volley was also described, composed of a long succession of sharp and low voltage peaks.     

Subpially recorded cervical spinal cord evoked potentials in syringomyelia.

Intraoperative spinal cord evoked potentials (SCEPs) to median nerve stimulation were detected subpially from the dorsal surface of the cervical spinal cord in 5 patients with cervical syringomyelia and were compared to normal SCEPs obtained from the unaffected side in 6 patients during intraoperative monitoring of dorsal root entry zone lesion. Normal SCEP began with a positive deflection P9 and a complex N11/N13 with several low amplitude short potentials superimposed on the N11/N13. The complex was followed by a second negative potential N2 and a late prolonged positivity, P. In the 4 patients in whom median nerve somatosensory evoked potentials (SEPs) were present preoperatively, SCEP consisted of the N11 potential and the following low amplitude short (LAS) potentials, while the N13 wave was missing. In the fifth patient, in whom the preoperative median nerve SEP was missing, SCEPs were of much lower amplitude and shorter duration than normal. The potentials N2 and P were not recorded in any of our 5 patients. Changes in N13 wave, N2 and P potentials noted in syringomyelia were presumed to be the result of destruction of the spinal cord dorsal horn neurons caused by spinal cord central cavitation.     

Skin and epidural recording of spinal somatosensory evoked potentials following median nerve stimulation: correlation between the absence of spinal N13 and impaired pain sense

Summary A clinical lesion study and intraoperative epidural recordings were made to test the origin and clinical significance of the spinal N13 and P13 of somatosensory evoked potentials (SEP) that follow median nerve stimulation. Intraoperatively, the respective peak latencies of spinal P13 and N13 coincided with those of the N1 component of the dorsal cord potential and its phase reversed positivity. On both the ventral and dorsal sides of the cervical epidural space, maximal amplitude was at the C5 vertebral level to which nerve input from the C6 dermatome is the main contributor. The modality of sensory impairment in the hand dermatome was examined in selected patients with cervical lesions, who showed such normal conventional SEP components as Erb N9, far-field P9, P11, P14, N18 and cortical N20, with or without loss of spinal N13. Statistically, the loss of spinal N13 was associated with decrease of pain sensation in the C6 dermatome. This was interpreted as being due to damage to the central grey matter of the cord, including the dorsal horn. Our results suggest the spinal N13 and P13 originate from the same source in the C6 spinal cord segment and that they are good indicators for the detection of centromedullary cervical cord damage.     

Simple measurement of spinal cord evoked potential: a valuable data source in the rat spinal cord injury model.

Measurement of spinal cord evoked potentials (SCEPs) is proposed as a means of predicting locomotion outcome in the rat spinal cord injury (SCI) model. Using 55 rats, three reproducible peak waves (waves I, II and III) were observed during stimulation at the C7 level with recording at the L1 epidural space. Hemisection at the T13 level showed three wave loss patterns: wave III loss only, loss of both wave II and III, and loss of all three waves. Defining an ideal SCI model as establishment of stable monoparesis or paraparesis, all animals in the wave II-III loss group showed favorable results. Histological data and electrophysiological properties allowed reasonable assumptions of wave origin: wave I from extrapyramidal tracts, wave II from the ventral corticospinal tract, and wave III from the dorsal corticospinal tract. Complete destruction of pyramidal tracts in both dorsal and ventral fibers was essential for long-term impairment of locomotion.     

Origin of components P 11 and P 13 in short latency somato-sensory evoked potentials (SSEP): correlative study of SSEP and intraoperative evoked potentials

In 15 patients with cervical or posterior fossa lesion, SSEPs were recorded between the skull and the non-cephalic reference electrodes during the surgical operation and compared with the evoked potentials directly recorded at the same time from the surface of the cervical spinal cord and the brain stem. The directly recorded evoked potential consisted of three main components appeared within about 25 ms., they were a small negative spike wave, a large positive spike wave and a subsequent slow potential. The positive spike wave of the evoked potentials recorded from the surface of the dorsal column was not only coincided in latency with component P 11 of SSEP, but also showed the greatest amplitude at the lower cervical level. Moreover, the positive spike wave gradually delayed in latency and reduced in amplitude from lower to upper cervical segments. The amplitude of the positive spike wave was greater at the surface of the dorsal column ipsilateral to the stimulated median nerve than that of contra-lateral recording. No polarity change was observed between the anterior and posterior surface of the spinal cord. Similarly, the positive spike wave of the evoked potentials, recorded from the surface of the brain stem, showed fairly same latency with P 13 and a maximal amplitude at the surface of the cuneate tuberculum ipsilateral to the median nerve stimulated, and those positive spike wave traveled to contra-lateral ventral surface of the pons, presumably from ipsilateral cuneate nucleus to the contra-lateral medial lemniscus.(ABSTRACT TRUNCATED AT 250 WORDS)     

Short-latency somatosensory evoked potentials in brain death

Summary Simultaneous recording of somatosensory evoked potentials to median nerve stimulation above the upper and lower neck in brain-dead patients revealed that all cervical responses were preserved in 10%, whereas a marked reduction in amplitude or even loss of N 13b at the level of the C2 spinous process was observed in 90%. Of the patients, 55% revealed an additional loss of N 13a, recorded at the level of the C7 spinous process; in 15% all cortical and spinal evoked potentials were missing, but Erb's point waves were still normal. These results suggest two different origins of the main negative waves (N 13a and N 13b), recorded above the upper and lower cervical spinal cord. N 13a (C7) is supposed to arise in the dorsal horn at the C6/7 level, N 13b (C2) in the cervicomedullary junction.     

Multiple-site optical recording reveals embryonic organization of synaptic networks in the chick spinal cord

We examined embryonic expression of postsynaptic potentials in stages 26-31 (E5 to E7) chick spinal cord slices. Slow optical signals related to the postsynaptic potentials which were evoked by electrical stimulation of afferent fibers were identified in the dorsal grey matter and the ventral motoneuronal area. In cervical spinal cord (C13) preparations, the dorsal slow signal appeared from stage 28 (E6), whilst the ventral slow signal was recognized from stage 29. At stages 26 and 27 (E5), no slow signal was observed in either the dorsal or ventral regions. On the other hand, in lumbosacral spinal cord (LS5) preparations, the dorsal, as well as ventral, slow signals appeared from stage 29; at stage 28 no slow signal was detected in the dorsal or ventral regions. These results suggest that there are differences in the ontogenetic expression of synaptic functions between the dorsal and ventral regions, and between the cervical and lumbosacral spinal cords. In embryos older than stage 29, removal of Mg2+ from the bathing solution markedly enhanced the amplitude and incidence of the ventral slow signal. In addition, in C13 preparations at stage 28, removal of Mg2+ elicited small slow signals in the ventral region in which no synaptic response was evoked in normal Ringer's solution. The slow signals induced in the Mg2+-free solution were blocked by 2-amino-5-phosphonovaleric acid (APV), showing that they are attributable to N-methyl- D-aspartate (NMDA) receptors. These results suggest that functional synaptic connections via polysynaptic pathways are already generated on motoneurons, but are suppressed by a Mg2+ block on the NMDA receptors at developmental stages when synaptic transmission from the primary afferents to the dorsal interneurons is initially expressed in the dorsal region.     

Epidurally recorded cervical somatosensory evoked potential in humans

Three slow wave components, P10, N13 and P18, can be seen in the cervical somatosensory evoked potential (CSEP) in response to median nerve stimulation recorded by an electrode in the epidural space at the dorsal aspect of the cervical spinal cord referenced to an electrode at the suprasternal notch. In the region of high CSEP amplitude, which extends over several cervical segments, the peak-to-peak amplitude is more than 10 microV, permitting observation of the CSEP slow waves in single, unaveraged records. The CSEP to finger nerve stimulation had a similar wave form and the same latencies (referred to the Erb's potential) as the CSEP to median nerve stimulation. The P10 activity is of presynaptic origin; it is generated in the brachial plexus, spinal roots and terminal branches of the primary sensory fibers. The N13 slow wave is of postsynaptic origin; however, the small wave on the ascending phase of this main postsynaptic component represents superimposed presynaptic activity. In bipolar epidural recordings, 3-5 fast waves are superimposed on the slow CSEP waves, which are of lower amplitude than the slow waves in unipolar recordings. The fast waves show a slight but progressive delay at the more rostral recording sites and are present even with high frequency stimulation, presumably reflecting activity in long ascending tracts. The surface recorded CSEP to median nerve stimulation is 4-7 times lower in amplitude than the CSEP in unipolar epidural recordings. The small wave on the ascending phase of N13 and the N13 peak of the unipolar epidural recordings had the same latencies as the surface N11 and N13 peaks.     

Optical imaging of spreading depolarization waves triggered by spinal nerve stimulation in the chick embryo: possible mechanisms for large-scale coactivation of the central nervous system

Using a multiple-site optical recording technique with a voltage-sensitive dye, we found that widely spreading depolarization waves were evoked by dorsal root stimulation in embryonic chick spinal cords. Spatiotemporal maps of the depolarization waves showed that the signals were mainly distributed in the ventral half of the slice, with the highest activity in the ventrolateral area. The propagation velocity of the waves was estimated to be in the order of mm/s. Depolarization waves were evoked in the ventral root-cut preparation, but not in the dorsal root-cut preparation, suggesting that the wave was triggered by synaptic inputs from the primary afferents, and that activation of the motoneurons was not essential for wave generation. In intact spinal cord-brain preparations, the depolarization wave propagated rostrally and caudally for a distance of several spinal segments in normal Ringer's solution. In a Mg(2+)-free solution, the amplitude and extent of the signals were markedly enhanced, and the depolarization wave triggered in the cervical spinal cord propagated to the brainstem and the cerebellum. The depolarization wave demonstrated here had many similarities with the vagus nerve-evoked depolarization wave reported previously. The results suggest that functional cell-to-cell communication systems mediated by the depolarization wave are widely generated in the embryonic central nervous system, and could play a role in large-scale coactivation of the neurons in the spinal cord and brain.     

Longitudinal distribution of negative cord dorsum potentials following stimulation of afferent fibres in the left inferior cardiac nerve

Cord dorsum potentials were recorded along the spinal cord following electrical stimulation of afferent fibres of the left inferior cardiac nerve in chloralose anaesthetized cats. The potentials were more pronounced in spinal than in intact cats. Afferent fibres which generated cord dorsum potentials in the cervical spinal cord were localized mainly in T2 and T3 and to a smaller extent in C8 and T1 dorsal roots. The responses consisted of two waves: with short (7.0 ms; N3 wave) and long (56 ms; N4 wave) latency to the onset of potentials. N3 and N4 waves were generated by group III and group IV afferent fibres, respectively. The N3 wave was maximal at C8 and T1 spinal cord level and could be detected at least 5-6 segments rostrally from the level of afferent input responsible for its generation. The N4 wave could be detected at least 4 segments rostrally from its afferent fibre input. We conclude that afferent fibres from the left inferior cardiac nerve activate neurones in the cervical spinal cord. The implications of such finding are discussed.     

Absence of spinal N13-P13 and normal scalp far-field P14 in a patient with syringomyelia

Short latency somatosensory evoked potentials to median or ulnar nerve stimulation were recorded in a patient with syringomyelia. Scalp-recorded far-field P14 was clearly preserved, but spinal N13-P13 components disappeared. Our findings support the hypothesis that spinal N13-P13 is generated by structures intrinsic to the cervical cord, most likely in the ventral central gray matter.     

Spinal cord electrical activity during focal depression of inhibitory processes]

Cord dorsum potentials, dorsal root potentials and field potentials were studied in rats with local depression of inhibitory processes in lumbar spinal segments produced by tetanus toxin. The study was carried out at a stage when excitation of a neuronal population with depressed inhibitory processes (the so-called "determinative dispatch station") evoked generalized excitation of spinal and bulbar motoneurons. In experiments with spinal animals it was shown that the stimulation of a cutaneous nerve on the affected side evokes DRP's P-waves and field potentials of greater amplitude and longer duration than those evoked on the opposite side or in healthy rats. The prolonged P-wave revealed several components which coinsided with prolonged ventral root discharges. This wave could be recorded from an enlarged spinal cord region. The maximal increased and prolonged negative field potentials corresponding in time to the enlarged P-wave were found in the ventral quadrant of the affected side. In this region "spontaneous" rhythmical negative slow waves were recorded. The mechanisms of spreading excitation from the site with depressed inhibitory processes and the localization of this site are discussed.     

Intra-operative spinal cord neuromonitoring in patients operated on for intramedullary tumors and syringomyelia

Intra-operative neuromonitoring is of great help to the neurosurgeon and enables him to operate more precisely and with less risk of post-operative neurological deficit. The purpose of the study was to define the changes of the somatosensory evoked potentials (SEP) elements in intramedullary tumors and syringomyelia, and to show the correlation between the changes of the elements and the location of the lesions in the spinal cord. Thirty patients with pain syndromes, intramedullary tumors and syringomyelia were operated on the spinal cord. The methodology of the intra-operative neuromonitoring was based on electrical stimulation of peripheral mixed nerve (tibial and median), and on intra-operative subpial recording of conducted and interneuronic SEP from the dorsal surface of the spinal cord. The recordings in pain syndrome cases were normal, and were compared with recordings obtained in syringomyelia and tumors. The most stable element of the conducted SEP are the initial negative waves that originate in the spinocerebellar tract. Deterioration of the negative high amplitude potentials is the most sensitive indicator of damage to the somatosensory system of the spinal cord, and indicates damage to the dorsal columns. The N11 and N14 waves are the most stable elements of the cervical and lumbosacral interneuronic SEP, and most probably originate in the dorsal root entry zone. Changes of the N13 and N17 elements of interneuronic SEP suggest damage to the spinal cord gray matter, and are most frequently changed in intramedullary lesions. High frequency waves seen on N13 or N17 probably reflect the somatosensory long tracts, and are even better seen in syringomyelia and pure intramedullary tumors. Changes in the elements of interneuronic and conductive SEP enable us to localize the anatomical site of the lesion, which is of great help to the operating neurosurgeon.     

Presynaptic modulation of synaptic effectiveness of afferent and ventrolateral tract fibers in the frog spinal cord

In the isolated frog spinal cord, antidromic stimulation of motor nerves produces intraspinal field potentials with a characteristic spatial distribution. When recording from the ventral horn, there is a short latency (1–2 msec) response corresponding to activity generated by antidromic activation of motoneuron cell bodies and proximal dendrites. In addition, in the dorsal horn, a delayed wave (12–13 msec latency) corresponding in time with the negative dorsal root potential is also recorded. This wave (VR-SFP) is positive at the dorsal surface of the cord and inverts to negativity at more ventral regions. The negative VR-SFP is maximum between 300–500 μm depth from the dorsal surface and decays with increasing depth towards the motor nucleus. Six days after chronic section of the dorsal roots L7 to L9 in one side of the spinal cord, stimulation of the motor nerves on the deafferented side produces only the early response attributable to antidromic activation of motoneurons. No distinctive VR-SFPs are recorded at any depth within the cord. These findings are consistent with the interpretation that afferent fiber terminals are the current generators of the VR-SFP. The presynaptic and postsynaptic focal potentials recorded in the motor nucleus after stimulation of the ventrolateral tract, as well as the corresponding synaptic potentials electrotonically recorded from the ventral roots, are not depressed during conditioning stimulations which produce primary afferent depolarization. This contrasts with the depression of the presynaptic and post-synaptic focal potentials and synaptic potentials produced by stimulation of sensory fibers. It is concluded that, unlike the afferent fiber terminals, the terminals of the ventrolateral tract are not subjected to a presynaptic modulation of the type involving primary afferent depolarization.     

Neurochemical and ionic mechanisms of dorsal root potentials in the spinal cord of the immature rat

Dorsal root potentials (DRP) recorded from spinal cord of 7-14-days old rats have two waves of depolarization. The fast wave of DRP is GABA-ergic in nature and the slow wave is evoked mainly by increasing of extracellular K+-ion concentration near the primary afferent terminals. The possible mechanisms of increasing extracellular K+-ion concentration evoked by dorsal root stimulation are discussed.     

Topographical organization of group II afferent input in the rat spinal cord

The organization of neurons in the lumbar enlargement of the rat spinal cord processing information conveyed by group II afferents of hind-limb muscle nerves has been investigated by using cord dorsum and intraspinal field potential recording. Group II afferents of different muscle nerves were found to evoke their strongest synaptic actions in specific segments of the lumbar cord. Group II afferents of quadriceps and deep peroneal nerves evoked potentials mainly at the rostral end of the lumbar enlargement (L1-rostral L3), whereas group II afferents of gastrocnemius-soleus and hamstring nerves evoked their main synaptic actions at the caudal end of the lumbar enlargement (L5). In the central lumbar segments (caudal L3–L4), the largest group II potentials were produced by afferents of tibialis posterior and, to a lesser degree, flexor digitorum longus. Field potentials evoked by group II afferents of quadriceps, tibialis posterior, and flexor digitorum longus were largest in the dorsal horn (up to 600 μV), but also occurred in the ventral horn where they were sometimes preceded by group I field potentials. In contrast, field potentials evoked by group II afferents of gastrocnemius-soleus and hamstring nerves were restricted to the dorsal horn. These results indicate that neurons in different segments of the rat lumbar spinal cord process information from group II afferents of different hind-limb muscles. Furthermore, the topographical organization of group II neuronal systems in the rat is similar in several respects to that in the cat and may therefore represent a general organizational feature of the mammalian spinal cord. J. Comp. Neurol. 394:357–373, 1998. © 1998 Wiley-Liss, Inc.     

Generators of human spinal somatosensory evoked potentials

Somatosensory evoked potentials recorded over the spine with a noncephalic reference following posterior tibial nerve stimulation have several components. (1) A stationary, synapse-dependent, negative potential (N22) occurs synchronously with a positive potential, P22, recorded ventral to the spinal cord and is localized to the lumbar region overlying the lumbar root entry zone. The N22/P22 complex is attributed to activation of interneurons in the dorsal gray of the lumbar cord. (2) A traveling negative potential with a gradually increasing latency may be recorded from the sacral to the cervical region. Its short refractory period indicates that it is not dependent on transmission across a synapse. This activity is attributed to transmission of the afferent volley through the lumbosacral plexus, roots, and the dorsal columns of the spinal cord. (3) N29, a stationary, synapse-dependent negative potential, localizes to the rostral cervical spine and is attributed to activation of the gracile nucleus relay cells. Following stimulation of the median nerve or fingers, the waveforms recorded over the cervical spine with a noncephalic reference include (1) the proximal plexus volley, a traveling negative potential reflecting transmission through the proximal brachial plexus and roots; (2) the dorsal column volley (DCV), the latency of which gradually increases from the caudal to rostral cervical region (the DCV is attributed to transmission of the afferent volley through the dorsal columns of the cervical cord); and (3) N13, a stationary negative waveform, with a long refractory period consistent with its dependence on transmission across a synapse. Experimental animal and human studies indicate that the N13 waveform is dependent on activity of at least two generator sites, namely the dorsal gray of the cervical cord and the cuneate nucleus.     

Changes in short latency SEPs (S-SEPs) to median nerve stimulation in brain dead patients

Short latency SEPs (S-SEPs) to median nerve stimulation consist of positive waves of P1, P2, P3 and P4, followed by negative waves of N 16 and N 19. These potential reflect activities of peripheral nerve, dorsal column of the cervical cord and medial lemniscus. The origins of these waves are considered as follows, P1--peripheral part of the brachial plexus, P2--the entry into the spinal cord or the dorsal column, P3--dorsal column nucleus or upper cervical cord, P4--the medial lemniscus, N 16--rostral brain stem or the thalamus, and N 19--thalamocortical projection or the cortex. The purpose of the present study is to elucidate changes of S-SEPs in brain dead patients. Fifteen brain dead patients were examined with S-SEPs. In addition to that, thirteen cases with lesions of subcortical or the brain stem but not in the state of brain death were studied for the controls. S-SEPs with non-cephalic references, conventional SEPs with earlobe reference and the evoked potentials at the Erb's point were recorded in all these cases. Serial recordings were performed in six brain dead cases during the process of rostro-caudal deterioration of the brain stem functions due to cerebral herniation. In the state of brain death, only P1 and P2 were recorded in eleven cases, and in three cases, only P1 was recorded. The other case with anoxic brain damage showed flat S-SEPs and the evoked potentials at the Erb's point could merely be obtained by the supramaximal stimulation.(ABSTRACT TRUNCATED AT 250 WORDS)     

Bit-mapped colour imaging of the potential fields of propagated and segmental subcortical components of somatosensory evoked potentials in man

Early somatosensory evoked potentials (SEPs) to median or ulnar nerve stimulation were recorded with non-cephalic reference from neck, oesophagus and scalp in normal young adults. Transit times and durations were estimated for different components. SEP fields were mapped with up to 24 skin electrodes around the neck or along the midline neck and scalp, and projected onto a 2-dimensional plane for bit-mapped colour imaging. The posterior neck N11 is a near-field potential propagated caudorostrally in the dorsal column, associated with a positive P11 far field beyond termination of the cuneate bundle. A true phase reversal of the posterior neck N13 into an anterior neck P13 is substantiated, identifying a segmental generator with horizontal axis in dorsal horn. The N13-P13 represents postsynaptic excitatory potentials in interneurones of layers IV-V of the dorsal horn. It is not reflected in any scalp far field. The duration and onset latency of N13-P13 are in line with this interpretation. A new montage of posterior-to-anterior neck can enhance this component without introducing extraneous potentials. The P14 far field does not extend below the inion and presents distinct features. Neck-to-front scalp montages confound the SEP components generated in the spinal cord and above the foramen magnum respectively, but may serve to estimate N11 onset latency.