The posterior root-muscle reflex

18.1

Introduction

Posterior root-muscle (PRM) reflexes are short-latency spinal reflexes evoked by the electrical stimulation of lumbar and upper sacral posterior rootles/roots and recorded from various lower limb muscles . Posterior root fibers can be stimulated in humans by electrodes surgically placed in the posterior epidural space [epidural spinal cord stimulation (SCS) ], by stimulating needle electrodes inserted into the epidural space , and by noninvasive electrical stimulation techniques using surface electrodes placed in a configuration to generate a current flow that partially passes the spinal canal (transcutaneous SCS ). PRM reflexes can be evoked in virtually all lower limb muscle groups bilaterally by a single stimulus pulse , because the lumbar and upper sacral posterior rootlets contain all proprioceptive afferent fibers from the legs and are densely arranged in bundles surrounding the posterior and posterolateral aspect of the spinal cord . In individuals with increased spinal excitability, a single stimulus pulse can elicit the short-latency PRM reflex and concomitantly longer latency reflexes or longer lasting afterdischarges . In this chapter, we will focus on short-latency PRM reflexes elicited by epidural and transcutaneous SCS . We will discuss the history of studies of PRM reflexes, the relevant neuroanatomy, methodological aspects of evoking PRM reflexes, and their physiological characteristics, specifically analogies and dissimilarities with respect to the H-reflex . Finally, we will give two examples of the use of PRM reflexes in intraoperative monitoring: (1) the neurophysiological assessment of epidural lead placement for the neuromodulation of lumbar sensory-motor circuits after spinal cord injury and (2) the neurophysiological assessment of the functional integrity of peripheral nerves supplying the legs during hip surgery.

18.2

History

The application of epidural SCS for the alleviation of disabilities following upper motor neuron lesions provided a novel opportunity to explore spinal cord physiology. Electrodes placed for therapeutic purposes could be used in parallel for recording cortically or peripherally evoked potentials or for eliciting responses in upper or lower limb muscles . Brief contractions in lower limb muscles (muscle twitches) in response to epidural lumbar SCS were already suggested in early neurophysiological studies to be initiated in proprioceptive afferent fibers within the posterior roots . Responses to train stimulation applied via posteriorly placed epidural electrodes demonstrated low-frequency depression , a hallmark of reflex responses , and must have thus been initiated in afferent fibers. Further, the responses were evoked, with their respective threshold intensities, in those muscles associated with the posterior roots closest to the stimulating epidural cathode . Computational and electromyography (EMG)-based studies provided further evidence that the evoked responses were initiated within proprioceptive afferents of posterior rootlets/roots. Meanwhile, neuroanatomical, physiological, and pharmacological animal experiments have provided more direct evidence that epidural lumbar SCS indeed evokes muscle responses through the electrical stimulation of afferent root fibers.

The short-latency reflex responses to SCS were termed PRM reflexes , according to their stimulation and recording sites and following the nomenclature of similar reflexes in classical electrophysiological studies in cat models (“dorsal-to-ventral root reflex” ; “dorsal root–ventral root reflex discharge” ). “Posterior” was favored over “dorsal” to emphasize that the PRM reflex is specific to human studies. In humans with the spinal cord in the upright anatomic position, posterior is synonymous with dorsal and anteroposterior is normally used for describing the axis connecting the front and the back . Finally, choosing this terminology helps to avoid confusion with “dorsal root reflexes,” which are antidromic action potentials in afferents originating in the spinal cord and propagating toward the periphery .

In parallel to epidural SCS, noninvasive electrical stimulation methods have been employed, initially to assess conduction in the lumbosacral roots. An early method, called high-voltage percutaneous electrical stimulation, used stimulators that were originally designed for transcranial electrical stimulation of the motor cortex, where high-intensity pulses were required to penetrate the cranium. Such stimulators generated spike-like pulses with durations of a few tens of microseconds, and maximal outputs of up to 1000 V . Small stimulating electrodes were placed longitudinally in bipolar configuration over the lumbar or sacral vertebrae, or monopolar stimulation was employed with one small active electrode overlying the spine, and the indifferent electrodes either over the iliac crest or the abdomen. EMG activity elicited by such stimulation could be recorded from various muscles of the lower limbs. In most muscles, these responses were M wave–like activities initiated in the motor axons, either intradurally within the anterior roots near the spinal cord or more distally at the intervertebral foramina. EMG recordings of soleus however indicated that larger diameter proprioceptive afferent fibers could be activated as well . This finding motivated the development of transcutaneous SCS . Based on biophysical and neurophysiological knowledge gained from studies using epidural SCS, and by employing stimulators that generate longer pulse widths to reduce stimulation thresholds and maximize the difference in the strength-duration properties of sensory and motor axons , a method was developed that can consistently evoke PRM reflexes in practically all lower limb muscles with moderate stimulation amplitudes .

Various other terminologies have been used for the PRM reflex in the literature. In initial neurophysiological studies utilizing epidural SCS in humans, PRM reflexes were described as “segmental muscle twitches” . In early studies using high-voltage percutaneous electrical stimulation, other investigators called the evoked responses “H-reflexes” . However, there are some physiological differences between the PRM reflex and the H-reflex, see later. Other terminologies used in studies of transcutaneous SCS were “multisegmental monosynaptic responses” , “root-evoked potentials” , and “trans spinal-evoked potentials” .

18.3

Anatomy of the posterior roots

Posterior root fibers are the proximal processes of the pseudounipolar sensory neurons, with their cell bodies located in the dorsal root ganglia (located outside the spinal canal within the intervertebral foramina) and their peripheral portion originating in the muscles, tendons, joints, and cutaneous and subcutaneous tissues of the body . Within the dural sac, each posterior root fans out into several rootlets, which enter the spinal cord in a longitudinal row at the posterolateral sulcus of their respective spinal cord segments. In the spinal cord the afferent terminals make synaptic contacts onto a vast number of homonymous and heteronymous spinal motoneurons and interneurons, which integrate supraspinal information to generate the final motor output . Caudally, the posterior roots follow a longitudinal component, which continues throughout the cauda equina. Average intrathecal root lengths increase from 61 mm for the L1 root to 159 mm for the S2 root . The lumbar roots exit the spinal canal with mediolateral orientations below their corresponding vertebrae through the intervertebral foramina. The S1 and S2 roots enter caudally into the sacral canal and exit through the anterior sacral foramina with a rather posteroanterior orientation.

The spatial arrangement of the posterior roots with respect to the anterior roots, which contain the motor axons, changes characteristically from the level of the spinal cord in caudal direction . At their respective segmental entry levels into the spinal cord, the posterior root fibers are separated from the anteriorly located motor fibers. Along the cauda equina, the posterior and anterior roots of the same segment approach each other to reach their common anterolateral sites of vertebral exits. Toward these exits, posterior and anterior roots of the same spinal cord segment are located close to each other and assume similar trajectories. These facts result in a spatial pattern of spinal root anatomy, and the evoked muscle responses reflect this characteristic anatomical arrangement , see also Section 18.5.3 .

18.4

Methodologies for evoking posterior root-muscle reflexes