Interactions between cutaneous and muscle afferent projections to cerebral cortex in man

In order to demonstrate interactions between cutaneous and muscle afferent volleys in the ascending somatosensory pathways, different nerves of the lower limb were stimulated together in a conditioning-test paradigm, the changes in the earliest component of the cerebral potential evoked by the test stimulus being taken to indicate such an interaction. It was first confirmed that the cerebral potential evoked by stimulation of the posterior tibial nerve at the ankle is derived from muscle afferents in the mixed nerve and has shorter latencies than the cerebral potential evoked by purely cutaneous volleys in the sural nerve (see Burke et al. 1981). Complete suppression of the cerebral potential evoked by stimulation of muscle or cutaneous afferents was produced by conditioning volleys in a different nerve or in a different fascicle of the same nerve. The major factors determining the degree of suppression were found to be the relative sizes of the conditioning and test volleys and their timing, rather than whether the volleys were of cutaneous or muscular origin. It is concluded that the transmission of cutaneous or muscle afferent volleys to cortex can be profoundly altered in normal subjects by conditioning activity. The possibility that normal background afferent activity can similarly modify afferent transmission has implications for diagnostic studies, particularly when they are performed under non-standard conditions, such as in the operating theatre or intensive care unit. It is also concluded that, although a subject may perceive cutaneous paraesthesiae when the posterior tibial nerve is stimulated at the ankle, there may be no cutaneous component to the evoked cerebral potential.     

The origins of lumbosacral spinal evoked potentials in humans using a surface electrode recording technique.

Somatosensory evoked potentials were recorded over the lumbar spine and scalp in 12 normal subjects after stimulating the posterior tibial nerve at the knee and ankle and the sural nerve at the ankle. The H-reflex from the soleus muscle was recorded at the same time. The effects of stimulus intensity, frequency of stimulation and vibration were assessed. It was concluded that when the posterior tibial nerve was stimulated in the popliteal fossa, three negative peaks were recorded over the lumbosacral area. They arose from activity in the dorsal roots, the dorsal horn of the spinal cord (SD) and the ventral roots. In contrast when the posterior tibial nerve and the sural nerve were stimulated at the ankle only two negative peaks were recorded, a dorsal root potential and a spinal cord dorsum potential. In addition the data suggested that the peripheral nerve fibres that are involved with generating the surface recorded spinal potential with mixed nerve stimulation are primarily muscle afferents.     

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.     

Are there motor fibers in the sural nerve?

A case of anomalous innervation of the abductor digiti quinti of the foot (ADQ) via the sural nerve is described. A muscle action potential from the ADQ could be elicited by stimulation of both the sural and the posterior tibial nerves.     

Posterior tibial and sural nerve somatosensory evoked potentials in dystrophia myotonica

Somatosensory evoked potentials (SEPs) were recorded in a group of 18 patients with dystrophia myotonica and in 28 control subjects after stimulating the right and left posterior tibial (SEP-PT) and sural (SEP-S) nerves at the ankles. Recording electrodes were placed in the popliteal fossae, overlying the L3 spinal vertebrae, and at the appropriate scalp sites. In all control subjects and dystrophia myotonica subjects SEP-PT latencies were shorter than equivalent SEP-S latencies, probably reflecting conduction along group I muscle afferents and along slower conducting cutaneous afferents, respectively. Intergroup comparisons revealed prolonged absolute and interpeak latencies in the dystrophia myotonica group, showing both peripheral and central somatosensory pathway involvement. Individual abnormal latencies which exceeded the control group mean plus 3 standard deviations were found in 66% of the dystrophia myotonica group, mainly due to prolonged peripheral conduction times. Results pointed to the concomitant involvement of both the posterior tibial and sural nerve somatosensory pathways in dystrophia myotonica.     

Magnetic stimulation of muscle evokes cerebral potentials

Somatosensory evoked potentials (SEPs) were recorded from the scalp in man to magnetic stimulation of various skeletal muscles. The potentials consisted of several components, the earliest of which decreased in latency as the stimulated site moved rostrally, ranging from 46 msec for stimulation of the gastrocnemius, to 14 msec for stimulation of the deltoid. Experiments were performed to distinguish the mechanisms by which magnetic stimulation of the muscle was effective in evoking these cerebral potentials. For the gastrocnemius, the intensity of the magnetic stimulus needed for evoking cerebral potentials was less than that required for activating mixed or sensory nerves in proximity to the muscle belly (eg, posterior tibial nerve in the popliteal fossa, sural nerve at the ankle). Vibration of the muscle or passive lengthening of the muscle, procedures which activate muscle spindles, were accompanied by a significant attenuation of the potentials evoked by magnetic stimulation of the muscle. Anesthesia of the skin underlying the stimulating coil had no effect on the latency or amplitude of the early components of the magnetically evoked potentials, whereas electrically evoked potentials from skin electrodes were abolished. Thus, the cerebral potentials accompanying magnetic stimulation of the muscle appear to be due to activation of muscle afferents. We suggest that magnetic stimulation of muscle can provide a relatively simple method for quantifying the function of muscle afferents originating from a wide variety of skeletal musculature.     

Idiopathic cortical myoclonus restricted to the lower limbs: correlation between MEPs and 99mTc-ECD single photon emission computed tomography activation study

We report a 63-year-old woman with cortical reflex myoclonus restricted to the bilateral lower limbs. Somatosensory evoked cortical potentials to posterior tibial nerve stimulation were enlarged with C-responses. Jerk-locked back averaging of the EEG identified a cortical spike related to myoclonic jerks. Motor evoked potentials recorded from the abductor hallucis muscle showed an exaggerated late response. These findings suggest hyperexcitability of the sensorimotor cortex. 99mTc-ECD single photon emission computed tomography (SPECT) after stimulation of the posterior tibial nerve showed increased perfusion in the contralateral peri-Rolandic area which corresponded to the hyperexcitable region. A SPECT activation study as well as MEPs therefore can be employed to determine the hyperexcitable region in cortical myoclonus.     

The relationship between the size of a muscle afferent volley and the cerebral potential it produces.

This study examined the relationship between the size of an afferent neural input produced by electrical stimulation of the posterior tibial nerve at the ankle and the size of the early components of the evoked cerebral potential. For five of six subjects the first peak of the afferent neural volley recorded in the popliteal fossa was uncontaminated by either motor efferents or cutaneous afferents. This was established by measuring the conduction times of motor fibres in the posterior tibial nerve and cutaneous fibres in the sural and posterior tibial nerves over the ankle to popliteal fossa segment. It is likely therefore that the first peak of the afferent volley contained predominantly, if not exclusively, activity in rapidly conducting afferents from the small muscles of the foot. The size of the two earliest components of the cerebral potential did not increase in direct proportion to the size of the afferent volley which produced it. The early components of the cerebral potential reached a maximum when the responsible muscle afferent volley was less than 50% of its maximum.     

Interfering cutaneous stimulation and the muscle afferent contribution to cortical potentials

Cerebral potentials were recorded in response to selective stimulation using microelectrodes of muscle afferents in motor fascicles innervating the intrinsic muscles of the foot or at the motor point of abductor hallucis. The early components of these potentials (P40, N50 and P60) were consistently attenuated by continuous tactile stimulation of related skin areas and by electrical stimulation of digital nerves, timed so that the digital volley reached cortex approximately 5 msec before the muscle afferent volley. The same conditioning cutaneous inputs also attenuated the cerebral potentials evoked by selective stimulation of cutaneous afferents. These findings confirm that there are intermodality and intramodality interactions between low-threshold cutaneous and muscle afferents and between cutaneous afferents, respectively. The findings indicate that 'interference phenomena' (Kakigi and Jones 1986) can occur between different afferent modalities, and within any one modality, and cannot be used to determine the afferent species responsible for the test evoked potential.     

Contribution of reference electrode to the compound muscle action potential

In compound muscle action potential (CMAP) recording, the contribution by the reference electrode is considered to be much smaller than that of the active electrode. We tested this assumption by making quantitative measurements of the signals recorded individually by the active and reference electrodes. In the thenar (median nerve) and extensor digitorum brevis (peroneal nerve) muscles, the reference electrode did contribute less. In the hypothenar muscle (ulnar nerve), however, the signals recorded by active and reference electrodes were of similar amplitude. In tibial nerve conduction studies (NCS), the CMAP from the abductor hallucis (AH) muscle was recorded mainly by the reference electrode; the large-amplitude signal recorded by the reference electrode is attributed to volume-conducted activity from other muscles stimulated during the study. The onset latency of the potential recorded by the active and reference electrodes was similar despite significantly different distances from the stimulating site. Hence, the merits of using anatomic landmarks for defining the distal stimulation site are assessed. When the reference electrode makes a large contribution, the CMAP amplitude may not decrease commensurate with any wasting of the muscle under the active recording electrode, and the need to use another muscle for recording the CMAP for that nerve should be considered.     

Recovery functions of common peroneal, posterior tibial and sural nerve somatosensory evoked potentials.

We studied recovery functions of the somatosensory evoked potentials (SEPs) of common peroneal (CPN), posterior tibial (PTN) and sural nerves (SN) using a paired conditioning-test paradigm. The interstimulus interval (ISI) of paired stimuli ranged from 2 to 400 msec. In all SEPs with ISIs of 12-20 msec, the amplitude recovery was close to or beyond 100% of the control response, though their latencies and wave forms were not the same as the control. Further increases of the ISI resulted in significant depression of SEP (late phase suppression), most markedly in CPN, and less prominently in SN-SEP. With a longer than 50 msec ISI there was progressive recovery of SEP, but full recovery differed depending on the nerve stimulated; 400 msec ISI was required for CPN-, 250 msec for PTN- and 100 msec for SN-SEP. The peroneal nerve block by local anesthetic injected just distal to the stimulus electrodes abolished the late phase SEP suppression observed before the nerve block. These findings suggest that the late phase SEP suppression is attributable to the "secondary" afferents as a result of activation of peripheral receptors (muscle, joint and/or cutaneous) by the efferent volley initiated from the stimulus point. The greater and longer duration of peripheral receptor activation in CPN than in PTN or SN stimulation could explain the more pronounced and the longer duration of late phase suppression in CPN-SEP.     

Medial dorsal superficial peroneal nerve studies in patients with polyneuropathy and normal sural responses

We studied medial dorsal superficial peroneal (MDSP) nerves in 52 patients with clinical evidence of mild chronic sensorimotor polyneuropathy and normal sural nerve responses, in order to assess the diagnostic sensitivity and usefulness of MDSP nerve testing in electrodiagnostic practice. To determine the effect of age on MDSP nerve parameters, 98 normal subjects were also examined. Electrodiagnostic evaluation involved studies of motor nerve conduction in tibial, peroneal, and median nerves; sensory nerve conduction in sural, MDSP, median, and radial nerves; tibial and peroneal nerve F waves; H reflexes from the soleus muscles; and needle electromyography of gastrocnemius and abductor hallucis muscles. Among the patients, 49% had low-amplitude sensory responses in MDSP nerves and 57% had either slowing of sensory conduction velocity or no sensory responses on proximal stimulation. MDSP nerve amplitude, tibial nerve motor velocity, and H reflexes were the most sensitive for detection of mild chronic symmetrical axonal sensorimotor polyneuropathy. MDSP nerve testing should be included in the routine electrodiagnostic evaluation of patients with suspected polyneuropathy and normal sural nerve responses.     

Effect of Agonist‐Antagonist Electrical Stimulation on Muscle Afferent Recordings in Anesthetized Rabbits

Objective. Sensory feedback extracted from muscle afferents is an approach to achieve closed‐loop control of paralyzed muscles using functional electrical stimulation (FES). The objective of the present study was to characterize the effect of agonist‐antagonist electrical stimulation on nerve cuff recordings of muscle afferent activity. Methods. Cuff electrodes were implanted around the tibial and peroneal nerve branches in five acute rabbit experiments. Two wires were implanted in each of the tibialis anterior (TA) and the lateral gastrocnemius (LG) muscles to obtain bipolar, intramuscular stimulation. Electroneurograms (ENG) were recorded during trapezoidal rotations of the ankle joint and compared during periods (25%, 50% and 100% of maximal force) with and without electrical stimulation of the muscle. Results. The activity from a stretched and electrically stimulated muscle showed the same pattern as the recordings from a matched nonstimulated muscle. The background afferent activity increased with increasing level of muscle stimulation. The static and dynamic sensitivities were not found to be different, except in one case (peroneal nerve at 100% TA recruitment). Discussion. The main contribution to the tibial activity was believed to originate from muscle afferents in nonstimulated, synergist muscles. The main contribution to the peroneal activity was believed to be from muscle afferents within the muscle being stimulated. It was suggested that the increased background activity could be attributed to the increased activity of the Golgi tendon organs. Conclusions. Sensory information about joint flexion and joint extension are preserved in muscle afferent recordings from electrically activated muscles at low and intermediate stimulation levels, but it still has to be shown whether muscle afferent information can be useful as sensory feedback in FES control.     

Parallel facilitatory reflex pathways from the foot and hip to flexors and extensors in the injured human spinal cord

Spinal integration of sensory signals associated with hip position, muscle loading, and cutaneous sensation of the foot contributes to movement regulation. The exact interactive effects of these sensory signals under controlled dynamic conditions are unknown. The purpose of the present study was to establish the effects of combined plantar cutaneous afferent excitation and hip movement on the Hoffmann (H) and flexion reflexes in people with a spinal cord injury (SCI). The flexion and H-reflexes were elicited through stimulation of the right sural (at non-nociceptive levels) and posterior tibial nerves respectively. Reflex responses were recorded from the ipsilateral tibialis anterior (TA) (flexion reflex) and soleus (H-reflex) muscles. The plantar cutaneous afferents were stimulated at three times the perceptual threshold (200 Hz, 24-ms pulse train) at conditioning-test intervals that ranged from 3 to 90 ms. Sinusoidal movements were imposed to the right hip joint at 0.2 Hz with subjects supine. Control and conditioned reflexes were recorded as the hip moved in flexion and extension. Leg muscle activity and sagittal-plane joint torques were recorded. We found that excitation of plantar cutaneous afferents facilitated the soleus H-reflex and the long latency flexion reflex during hip extension. In contrast, the short latency flexion reflex was depressed by plantar cutaneous stimulation during hip flexion. Oscillatory joint forces were present during the transition phase of the hip movement from flexion to extension when stimuli were delivered during hip flexion. Hip-mediated input interacts with feedback from the foot sole to facilitate extensor and flexor reflex activity during the extension phase of movement. The interactive effects of these sensory signals may be a feature of impaired gait, but when they are appropriately excited, they may contribute to locomotion recovery in these patients.     

The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord

Transganglionic transport of wheatgerm agglutinin conjugated horse-radish peroxidase (WGA-HRP) was used to reveal the central distribution of terminals of primary afferent fibers from peripheral nerves innervating the hind leg of the rat. In separate experiments the sizes and locations of cutaneous peripheral receptive fields were determined by electrophysiological recording techniques for each of the nerves that had been labeled with WGA-HRP. By using digital image analysis, the sizes and positions of the peripheral receptive fields were correlated with the areas of superficial dorsal horn occupied by terminals of primary afferents from each of these receptive fields. Data were obtained from the posterior cutaneous nerve of the thigh, lateral sural, sural, saphenous, superficial peroneal, and tibial nerves. The subdivisions of the sciatic nerve, the sural, lateral sural, superficial peroneal, and tibial nerves each projected to a separate and distinct region of the superficial dorsal horn and collectively formed a "U"-shaped zone of terminal labeling extending from lumbar spinal segments L2 to the caudal portions of L5. The gap in the "U" extended from L2 to the L3-4 boundary and was occupied by terminals from the saphenous nerve. Collectively, all primary afferents supplying the hindlimb occupied the medial 3/4 of the superficial dorsal horn with terminals from the tibial nerve lying most medially and occupying the largest of all the terminal fields. Afferents from the superficial peroneal lay in a zone between the medially situated tibial zone and the more laterally placed sural zone. Afferents from the posterior cutaneous nerve were located most caudally and laterally. Terminal fields from the posterior cutaneous and saphenous nerves differed from the others in having split representations caused presumably by their proximity to the mid-axial line of the limb. Comparisons between the peripheral and the central representations of each nerve revealed that 1 mm2 of surface area of the superficial dorsal horn serves approximately 600-900 mm2 of hairy skin and roughly 300 mm2 of glabrous skin. The vast majority of terminal labeling observed in the dorsal horn was found in the marginal layer and substantia gelatinosa, suggesting that small diameter afferents have an orderly somatotopic arrangement in which each portion of the skin surface is innervated by afferent fibers that terminate in preferred localities within the dorsal horn.     

Reduced sensory and motor conduction velocity in 25-week-old diabetic [ ] mice

Motor and sensory conduction velocities were measured in sural and tibial nerves of 25-week-old genetically diabetic ( ) mice and their nondiabetic littermates. For motor conduction velocity determination, the sciatic nerve was stimulated at the hip and the tibial nerve subsequently stimulated at the ankle while recording interosseous muscle potentials from needle electrodes placed in the foot. Sensory conduction velocities were determined by recording compound action potentials directly from sural and tibial nerves at the ankle after sciatic nerve stimulation. Control and diabetic conduction velocities were compared by Student's t test. The motor conduction velocity was reduced by approximately 20% from the control, and the distal motor latency was increased in mice by 22% more than the control latency. Conduction velocity was also reduced in some sensory fibers, an observation not previously reported in the mouse. Sensory fibers most severely affected were the faster-conducting fibers of the sural nerve, whose conduction velocity was decreased by 18% from the control. Slower-conducting sensory fibers in sural and tibial nerves were only midly affected, whereas fast-conducting sensory fibers of the tibial nerve appeared to remain normal. These data suggest that not all nerve fibers react alike to the diabetic state in the genetically diabetic ( ) mouse.     

The latency difference of the tibial and sural nerve SEP: peripheral versus central factors

The latency of the cortical SEP (CSEP) following stimulation of the posterior tibial nerve is nearly always shorter than the latency of the CSEP evoked by stimulation of the sural nerve. Till now this fact was believed to be due mainly to different conduction velocities within the peripheral nerves owing to the muscle afferents of the posterior tibial nerve. The surprising discovery that the lumbar and cervical SEPs exhibit much shorter time lags than the CSEPs led to the experiments described in this paper: during the registration of the peripheral sciatic nerve action potentials only slight differences in the conduction velocities were observed. Thereupon a topographical analysis was performed during which the minimum latency of the sural nerve CSEP was not measured at the usual C'z electrode position but was found to be shifted to a more occipital and ipsilateral point. From these results it was concluded that, for the main part, the latency difference of the CSEPs results from 'central factors,' which had already been postulated for the median nerve CSEP by Burke and coworkers.     

On the cause of hyporeflexia in the Holmes-Adie syndrome

Electrophysiologic studies were carried out on 11 patients with Holmes-Adie syndrome, 8 of whom had reduced or absent ankle jerks. Conduction velocities and evoked nerve and muscle compound action potentials in the peroneal, posterior tibial, and sural nerves were normal. The H reflex was absent (or virtually absent) in the patients with depressed reflexes. The amplitude of the composite Ia EPSP in single soleus motoneurons was estimated from changes in firing probability of voluntarily activated soleus motor units in response to stimulation of low threshold afferents in the tibial nerve. These amplitudes were used to test the afferent side of the reflex pathway. Composite group Ia EPSPs in Holmes-Aide patients with hyporeflexia were smaller than normal or absent, indicating that the areflexia in the Holmes-Aide syndrome is due to loss of large spindle afferents or reduced effectiveness of their monosynaptic connections to motoneurons.     

Proximal and segmental motor nerve conduction in the sciatic nerve produced by percutaneous high voltage electrical stimulation

Percutaneous high voltage electrical stimulation was applied to the proximal sciatic nerve at the hip in 18 normal subjects to evaluate motor conduction in the proximal sciatic nerve, and short-segment stimulation of the sciatic and posterior tibial nerves was given in 6 normal subjects. Compound muscle action potentials (CMAPs) were recorded from the abductor hallucis (AH) and extensor digitorum brevis (EDB) muscles. Supramaximal stimulation was easily obtained at the proximal sciatic nerve and all the sites in the short-segment stimulation. The motor nerve conduction velocity of the sciatic nerve between the hip and the popliteal fossa was 49.2 ± 4.24 m/sec in the tibial division and 54.1 ± 6.48 m/sec in the peroneal division. The respective peak-to-peak amplitude and negative-peak areas of the CMAPs at the hip were reduced to 86.8 ± 5.65% and 97.3 ± 5.36% for the tibial division, and 93.4 ± 7.06% and 96.8 ± 5.09% for the peroneal division as compared to the values for the popliteal fossa. The negative-peak duration of the CMAPs at the hip point were increased to 109.2 ± 7.2% for the tibial nerve and 107.1 ± 5.68% for the peroneal nerve as compared with the duration at the popliteal fossa. This method is non-invasive and useful for evaluating motor nerve conduction in the lower limb.     

Modality-related scalp responses after electrical stimulation of cutaneous and muscular upper limb afferents in humans

To elucidate whether the selective electrical stimulation of muscle as well as cutaneous afferents evokes modality-specific responses in somatosensory evoked potentials (SEPs) recorded on the scalp of humans, we compared scalp SEPs to electrical stimuli applied to the median nerve and to the abductor pollicis brevis (APB) motor point. In three subjects, we also recorded SEPs after stimulation of the distal phalanx of the thumb, which selectively involved cutaneous afferents. Motor point and median nerve SEPs showed the same scalp distribution; moreover, very similar dipole models, showing the same dipolar time courses, explained well the SEPs after both types of stimulation. Since the non-natural stimulation of muscle afferents evokes responses also in areas specifically devoted to cutaneous input processing, it is conceivable that, in physiological conditions, muscle afferents are differentially gated in somatosensory cortex. The frontocentral N30 response was absent after purely cutaneous stimulation; by contrast, it was relatively more represented in motor point rather than in mixed nerve SEPs. These data suggest that the N30 response is specifically evoked by proprioceptive inputs.