Conduction characteristics of somatosensory evoked potentials to peroneal, tibial and sural nerve stimulation in man

Lumbar spine and scalp short latency somatosensory evoked potentials (SSEPs) to stimulation of the posterior tibial, peroneal and sural nerves at the ankle (PTN-A, PN-A, SN-A) and common peroneal nerve at the knee (CPN-K) were obtained in 8 normal subjects. Peripheral nerve conduction velocities and lumbar spine to cerebral cortex propagation velocities were determined and compared. These values were similar with stimulation of the 3 nerves at the ankle but were significantly greater with CPN-K stimulation. CPN-K and PTN-A SSEPs were recorded from the L3, T12, T6 and C7 spines and the scalp in 6 normal subjects. Conduction velocities were determined over peripheral nerve-cauda equina (stimulus-L3), caudal spinal cord (T12-T6) and rostral spinal cord (T6-C7). Propagation velocities were determined from each spinal level to the cerebral cortex. With both CPN-K and PTN-A stimulation the speed of conduction over peripheral nerve and spinal cord was non-linear. It was greater over peripheral nerve-cauda equina and rostral spinal cord than over caudal cord segments. The CPN-K response was conducted significantly faster than the PTN-A response over peripheral nerve-cauda equina and rostral spinal cord but these values were similar over caudal cord. Spine to cerebral cortex propagation velocities were significantly greater from all spine levels with CPN-K stimulation. These data show that the conduction characteristics of SSEPs over peripheral nerve, spinal cord and from spine to cerebral cortex are dependent on the peripheral nerve stimulated.     

Spinal somatosensory evoked potentials in juvenile diabetes

Spinal somatosensory evoked potentials to stimulation of the peroneal nerves in the popliteal fossa were recorded from 46 insulin-dependent neurologically normal patients with juvenile diabetes. Conduction velocities of these potentials were determined over proximal peroneal nerve, cauda equina, and spinal cord and were compared with those obtained from 46 age-matched control subjects. Mean values for overall spinal conduction velocity (L3-C7 spines) and conduction velocity over rostral spinal cord (T6-C7 spines) and peroneal nerve-cauda equina (stimulus to L3 spine) were lower in the diabetic group (p less than 0.001). Peripheral nerve conduction velocity alone was slow in 5 patients, and spinal conduction velocity was slow in 8; in 2 patients both peripheral and spinal velocities were slow. This study suggests that in addition to impairment of peripheral nerve function, patients with juvenile diabetes without clinical evidence of neurological involvement can have a defect in spinal afferent transmission.     

Cerebral and spinal somatosensory evoked potentials in children with CNS degenerative disease

Spinal and cerebral somatosensory evoked potentials to peroneal nerve and median nerve stimulation were recorded in 17 children with CNS degenerative disease and compared with similar potentials obtained in a group of age-matched normal control subjects. Spinal potentials were increased in duration over caudal cord segments and were poorly defined or absent over the rostral cord in some patients. In 12 patients the conduction velocity of the spinal response was slow over spinal cord segments. However, conduction velocity over peripheral nerve and cauda equina was normal in all patients. The scalp recorded evoked potentials to both median and peroneal nerve stimulation which arise in neural structures rostral to the brain stem were absent in 14 patients. Cerebral responses and certain spinal potentials were greatly increased in amplitude in one patient with myoclonus. This study demonstrates that these methods permit an evaluation of the entire neuraxis from peripheral nerve to cerebral cortex and that they may be helpful in the evaluation of patients with diffuse or multifocal disease of the nervous system.     

The spinal evoked response in infants and children.

Summated responses to peroneal nerve stimulation were recorded from surface electrodes placed over the spine of 60 infants and children. These potentials generally were greater in amplitude in infants than in older children. Over the cauda equina and rostral cord, initially positive triphasic potentials were recorded. Over the caudal cord, complex potentials were recorded in children less than three years of age. The conduction velocity of the response from midlumbar to lower cervical recording sites was less in infants than in older children and progressively increased with age, reaching adult values after the fourth year.     

Maturation of somatosensory evoked potentials upon posterior tibial nerve stimulation

Somatosensory evoked potentials produced in response to posterior tibial nerve stimulation were studied in 42 normal infants and children, ages 4 months to 16 years. The maturation of afferent conduction from the lower limb was evaluated for the peripheral nerve, spinal cord, and central nervous system. Although the maturation of conduction in the peripheral nerve (from the ankle to the popliteal fossa and from the popliteal fossa to L₃) was complete by 6 years of age, afferent conduction in the spinal cord (from L₃ to C₇) was not complete until 12 years of age or older. Spinal evoked potentials investigated in the thoracolumbar area revealed a phase-reversed potential located between the lower thoracic spine and upper lumbar spine in over 80% of patients. Reciprocal velocities for the major cortical positive potential P₁ (corresponding to P₃₇ in adults) and its onset, N₁, steadily decreased with age and leveled off at greater than 12 years of age and by 12 years of age, respectively. The propagation velocity from L₃ to the cerebral cortex also increased steadily with age, leveling off at greater than 12 years of age. Accordingly, the maturation of afferent conduction in the central nervous system was not complete until affer 12 years of age.     

Intraoperative recordings of spinal somatosensory evoked potentials to tibial nerve and sural nerve stimulation

Somatosensory evoked potentials (SSEPs) to stimulation of the tibial nerve at the knee (TN-K) and ankle (TN-A), and the sural nerve at the ankle (SN-A), were recorded from 3 or 4 spinal levels during surgery for scoliosis in 11 neurologically normal subjects. With stimulation of all 3 nerves, the propagation velocity along the spine was nonlinear: it was faster over cauda equina and midthoracic cord than over caudal spinal cord. Over the mid-thoracic cord, TN-K SSEP propagation was faster than that of TN-A and SN-A SSEPs, whereas over the caudal spinal cord these values were similar on stimulation of all 3 nerves. These data suggest that fast conducting second order afferent fiber systems contribute to spinal cord SSEPs evoked by stimulating both mixed and cutaneous peripheral nerves.     

Spinal evoked potential in the monkey

Computer-averaged evoked potential responses (EPs) to stimulation of the sciatic nerve and cervical spinal cord were recorded from the dura and skin over the cauda equina and spinal cord in seven monkeys, three with chronic spinal cord lesions. Sciatic EPs consisted of predominantly negative triphasic propagated potentials recorded at all spinal levels and greatest in amplitude over the cauda equina and caudal spinal cord. The conduction velocity of this EP was faster over the cauda equina and rostral spinal cord than over caudal cord segments. Triphasic potentials were succeeded by small negative potentials over the cauda equina and larger negative potentials over the lumbar enlargement. Sciatic EPs over the upper lumbar and thoracic cord were more sensitive to asphyxia than the initial triphasic potentials recorded over cauda equina and caudal cord but resisted changes from increasing the rate of stimulation up to 100 per second. Propagated thoracic EPs were preceded by nonpropagated potentials. The longer latency negative potentials occurring locally over the cauda equina and lower lumbar enlargement were abolished at levels of asphyxia and were attenuated at rates of stimulation that did not affect the preceding triphasic potentials. Following complete spinal cord transection, nonpropagated sciatic EPs were recorded in leads rostral to the section. In preparations with chronic partial cord hemisection involving dorsal and lateral quadrants, ipsilateral sciatic EPs had increased latency, reduced amplitude, and poor definition in the vicinity of and rostral to the lesion. Direct cervical cord stimulation elicited caudally propagated potentials which were followed by large, broad potentials over the lumbar enlargement.     

Evoked potentials recorded from scalp and spinous processes during spinal column surgery

Peroneal nerve evoked potentials were simultaneously recorded from scalp and from wire electrodes inserted into lumbar and thoracic spinous processes at multiple levels during surgery for correction of spinal column curvature in 43 patients. Spinal potentials progressively increased in latency rostrally. Over cauda equina and rostral spinal cord initially positive triphasic potentials were recorded. Over caudal spinal cord the response consisted of initial positive-negative diphasic potentials that merged with broad large negative and positive potentials. At rapid rates of stimulation, the initial diphasic component was stable but the subsequent potentials significantly diminished in amplitude. This suggests that the diphasic component reflects presynaptic activity arising in the intramedullary continuations of dorsal root fibers and that the subsequent components reflect largely postsynaptic activity. Scalp recordings at restricted bandpass (30-3000 c/sec) revealed well defined positive and negative potentials with mean peak latencies of 25.9 and 29.9 msec (PV-N1). The amplitudes and latencies of PV-N1 remained relatively stable throughout general anesthesia with halogenated agents which suggests that this component may be a reliable monitor of conduction within spinal cord afferent pathways during spinal surgery. Data are presented which suggest that selective filtering may help to distinguish faster frequency, synchronous axonal events from slower frequency, asynchronous axonal or synaptic events.     

Short latency somatosensory evoked potentials following the peripheral nerve stimulation of lower extremities in children

We have evaluated the short latency somatosensory evoked potentials (SSEPs) following peroneal and posterior tibial nerve stimulation in 27 normal children and adults, and then applied SSEPs examination following peroneal nerve stimulation to 6 children with neurological deficits. Features of the evoked potentials following peroneal nerve stimulation in normal children were almost similar to those in adults, but we found several points characteristic in children; a higher incidence of evoked potentials and a clearer appearance of "standing potential" at the lower thoracic vertebral level than in adults. Spinal afferent conduction velocity reached at a maximum at 3-4 years of age. The SSEPs following peripheral nerve stimulation in lower extremities are useful in pediatric neurology to determine the level of the spinal lesion, to reveal the distribution and pathophysiology of the spinal dysfunction, and to analyze the process of the disease progression.     

Spinal cord representation of the micturition reflex

The spinal cord origin and peripheral pathways of the sensory and motor nerves to the urinary bladder were delineated in the cat by stimulating the appropriate nerves near the urinary bladder and recording from the dorsal and ventral rootlets near the spinal cord. The parasympathetic preganglionic neurons originated in the sacral segments of the spinal cord and reached the bladder by way of the pelvic nerve. The preganglionic parasympathetic perikarya to the urinary bladder were distributed over a length of approximately 1.5 segments, centered near the junction of segments S-2 and S-3 in cats with a median arrangement of the lumbosacral plexus. Conduction velocities in preganglionic parasympathetic fibers to the bladder ranged from 46 to 2 M/sec with a mean maximal velocity of 18.2 M/sec. The major sympathetic pathway to the bladder was in the hypogastric nerve. Preganglionic sympathetic fibers originated in the lumbar spinal cord and traveled through the caudal mesenteric ganglion and hypogastric nerve to the urinary bladder. There were both ipsilateral and contralateral preganglionic and afferent fibers in this pathway. The preganglionic sympathetic neurons originated in segments L-2 and L-5. They were usually distributed over approximately 2 full segments centered near the junction of L-3 and L-4 in cats with a median arrangement of the lumbosacral plexus. Neurons involved in the micturition reflex may extend from the rostral end of the L-2 segment to the caudal end of the S-3 segment. The sympathetic preganglionic neurons were usually separated from the somatic and parasympathetic columns by segments L-5 to L-7.     

Nerve impulse propagation along central and peripheral fast conducting motor and sensory pathways in man

Forty-four limbs from 11 healthy volunteers were examined. Spinal and scalp somatosensory evoked potentials to median and peroneal nerve stimulation were recorded and the peripheral (wrist-Erb, Erb-cervical, knee-thoracic spine) and central (cervical-scalp, thoracic-cervical spine, spine-scalp) conduction times and velocities (CTs, CVs) were calculated. Sensory and mixed trunks of median and peroneal nerves were also stimulated and their motor and sensory CVs in mid-distal districts were measured. Motor responses to scalp (motor areas for hand and leg muscles) and spinal cord stimulation (cervical and lower thoracic levels) were carried out through skin rectangular plate electrodes delivering high voltage (880-1870 V) brief anodal pulses. The intracranial (scalp-cervical) and intraspinal (cervical-thoracic spine) CTs and CVs of motor pathways were measured. The elbow-cervical and knee-thoracic spines CTs of motor fibres were also calculated through the F wave method, which gave values almost superimposable on those obtained through direct spine stimulation. Nerve propagation was faster in sensory than in motor fibres in peripheral nerve mid-distal districts, while this difference was reduced or reversed in more proximal segments, including nerve roots. The scalp-cervical CT was slightly shorter in motor than in sensory fibres after subtraction of synaptic delays (6.12 vs. 6.18 msec). The scalp-lower thoracic spine, as well as the intraspinal, CVs were 7-12% faster in sensory than in motor pathways (45.3 vs. 38.7 m/sec for the former; 62.65 vs. 55.4 m/sec for the latter). The reported method allows the evaluation of fast conducting motor and sensory pathways along 'central' and 'peripheral' nerve structures of the entire body. Preliminary findings on scalp stimulation of brain motor areas with low voltage pulses are also included.     

Spine and scalp somatosensory evoked potentials in normal subjects and patients with spinal cord disease: evaluation of afferent transmission

Spine and scalp somatosensory evoked potentials (SEPs) to peroneal nerve stimulation were recorded from 20 normal subjects using 1 restricted and 3 open frequency filter bandpasses. Spine to spine and spine to scalp propagation velocities were calculated. Of those recording parameters investigated, optimal recordings were obtained using an open bandpass (5-1500 or 30-1500 Hz) and recording from 3 surface spine bipolar channels and 1 scalp bipolar channel. This method was then investigated in 40 patients with disease of the spinal cord and peripheral nervous system. Focal spinal cord compressive lesions generally resulted in slowing of spine to spine and spine to scalp propagation velocities. Diffuse or multifocal lesions of the spinal cord generally resulted in the absence of scalp responses. Although there was no consistent correlation of the SEP findings with the sensory exam, there was a correlation of the SEP findings with the clinical prognosis.     

Central vs peripheral nerve conduction. Before and after treatment of subacute combined degeneration

Central and peripheral nerve conduction was studied in two patients with subacute combined degeneration by using the short-latency somatosensory evoked potentials and the peripheral nerve conduction study during treatment with cyanocobalamin. Before the treatment, somatosensory evoked potentials with median nerve stimulation were normal, but those with peroneal nerve stimulation revealed prolonged central conduction indicating dysfunction within the posterior column. Peripheral sensory and motor nerve action potentials were reduced with normal or slightly reduced conduction velocity. After treatment, marked shortening of the central conduction time (by 24% and 31%, respectively) was observed with mild or no recovery of peripheral nerve action potentials. These physiologic findings suggest that the main pathologic changes in the central nervous system may be demyelination in the posterior column in addition to axonal degeneration in the peripheral nerve. The former was responsive to treatment but the latter was poorly responsive to treatment. Sensory symptom in subacute combined degeneration appears to be, at least partially, attributed to the spinal cord lesion.     

Spinal sympathetic conduction velocity in humans

Simultaneous micro-electrode recordings of muscle sympathetic activity were made in the radial nerve at the mid-humerus level and the peroneal nerve at the fibular head in 8 healthy subjects. Sympathetic impulses occurred spontaneously in multi-unit bursts time-locked to the cardiac rhythm. There was a high degree of similarity between radial and peroneal neurograms with the radial bursts preceding corresponding peroneal ones by approximately 0.35 s. Utilizing this latency difference and previously determined values for peripheral sympathetic postganglionic conduction velocities, we calculated that the spinal conduction velocity for muscle sympathetic activity is 2.8 +/- 0.7 m/s (mean +/- SD). The result agrees with similar data from experimental animals.     

Conduction properties of epidurally recorded spinal cord potentials following lower limb stimulation in man

Spinal somatosensory evoked potentials were recorded in 35 neurologically normal patients undergoing surgery for scoliosis. During posterior procedures the recording electrodes were placed in the dorsal epidural space and during anterior operations in the intervertebral discs. Stimulation was of the tibial nerve in the popliteal fossa and the posterior tibial and sural nerves at the ankle. At thoracic levels the response consisted of at least 3 components with different peripheral excitation thresholds and spinal conduction velocities (range 35-85 m/sec). All components were conducted mainly in tracts ipsilateral to the stimulus, component 1 being most laterally located. At low stimulus intensity only the fastest activity was recorded but this was markedly delayed over low thoracic segments and was recorded as a repetitive discharge rostrally. Higher intensities elicited additional components which were conducted at a slower but relatively uniform velocity; consequently they might overlap with or even overtake the fast activity at mid-to-low thoracic levels. Component 1 was much less prominent when the posterior tibial nerve was stimulated at the ankle and absent from the (cutaneous) sural nerve response; remaining potentials were conducted at velocities similar to those of components 2 and 3 following tibial nerve stimulation at the knee. Small 'stationary' potentials were recorded at all thoracic levels, probably due to the change in conductivity as the volley entered the spinal cord. Efferent activity was recorded at and below the thoraco-lumbar junction, possibly related to the H-reflex or F-wave. Similar, although smaller, afferent potentials were recorded from the anterior side of the vertebral column. Component 1 is likely to be due to the stimulation of group 1 muscle afferents which terminate in the dorsal horn and activate second order neurones, many of whose axons go to form the ipsilateral dorsal spinocerebellar tract. Components 2 and 3 are believed to be largely cutaneous in origin and to be conducted mainly in the dorsal columns.     

Noninvasive measurement of central sensory and motor conduction

Potentials evoked by median and peroneal nerve stimulation were digitally filtered between 300 and 2,500 Hz to measure early latency components and assess sensory cord conduction velocity. Short (R1) and long (R2) latency reflex responses were recorded from contracting thenar and tibialis anterior muscles. R1 is considered a spinal reflex akin to the H-reflex. Clinical evidence suggests that R2 involves a reflex arc with turnaround at the motor cortex. Sensory-motor cord velocity was derived from the latencies of R1 and R2. The method can be used to compare peripheral and central sensory conduction or conduction in central sensory and motor pathways.     

Congenital caudal spinal atrophy: a case report.

An infant presented at birth with symmetrical flaccid paraparesis limited to lower legs and feet, and involving the proximal and distal muscle group. Limitation of the ankle joints was noticed. There were no sensory deficits to painful stimuli and no evidence of loss of sphincter control. Muscle CT revealed severe muscle atrophy in the pelvis and lower limbs, and electromyographic study of the bilateral hamstrings showed polyphasic giant potentials. Motor and sensory nerve conduction velocities were within normal limits, and the spinal MRI showed no structural abnormalities in the cord and the lower spine. These features suggest a congenital segmental abnormality at the anterior horn cell level in the lumbosacral spinal cord, which we propose to call "congenital caudal spinal atrophy".     

Neural and anatomic characteristics of peripheral afferent fibers in the milk ejection reflex

Conduction velocities were measured and certain morphologic characteristics were examined of the abdominal mammary nerve in two- to ten-day postpartum rats. This nerve enters the spinal cord at the spinal segmental level T-12. Overall conduction velocity was (Mean +/- S.D.) 18.9 +/- 2.25 m/sec with a major peak at 9.7 +/- 0.72 m/sec. The distribution of conduction velocities in the nerve was similar to that of a typical spinal nerve. Nerve fiber diameters measured between about 1 and 25 microns with peaks at 4.9, 10.5, and 18.9 microns. Injection into the peripheral nerve of fluorescent dye, Lucifer yellow CH (LY), or wheat germ agglutinin-coupled horseradish peroxidase (WGA-HRP) after ventral root rhizotomy permitted study of the distribution of primary afferents in the spinal cord. The terminal field of these fibers centered around the dorsal cap of Clarke's column and the lateral spinal nucleus, bilaterally. The distribution of WGA-HRP was more restricted than that of LY. A large number of LY-staining fibers were also found ipsilaterally in the medial portion of the intermediomedial column. A smaller amount of LY-staining was present contralaterally in the area of the spinothalamic tract. It is concluded that afferent impulses resulting from mammary stimulation in the milk ejection reflex are probably carried in a mixed spinal nerve whose primary afferent field lies mainly in ipsilateral spinal structures, although there is some evidence for crossing fibers. The data suggest that considerable opportunity exists for interaction with major sensory afferent fiber systems as well as with autonomic fibers. Hence, the spinal path of afferent information relevant for the milk ejection reflex may well be diffuse and it may involve several sensory modalities.     

Short latency potentials recorded from the neck and scalp following median nerve stimulation in man.

Short latency evoked potentials were recorded from sites overlying the cervical and thoracic vertebrae, the clavicles, mastoid processes and cerebral cortex, following percutaneous stimulation of median nerve fibres at the elbow, wrist and fingers in 23 normal subjects. At least four major early components each with simultaneous positive and negative constituents, plus the first component (N20) of the cortical response, were all found to be mediated by sensory afferent fibres with conduction velocity 65--75 m/sec in the forearm of one subject. Study of the distribution of these potentials, using reference electrodes located at Fz or over the lower part of the spine, has led to the proposal of generator sites in the brachial plexus (N9), spinal roots or dorsal columns (N11), spinal grey matter or brain stem (N13), and brain stem or thalamus (N14). Comparison with intrathecal recordings in man lends support to the view that N11 and N13 are generated in or adjacent to the spinal cord. It is hoped the findings may extend the clinical applications of a non-invasive technique for investigating the afferent sensory pathways in man.     

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.