Damage to the corticospinal tract is a leading cause of motor disability, for example in stroke or spinal cord injury. Some function usually recovers, but whether plasticity of undamaged ipsilaterally descending corticospinal axons and/or brainstem pathways such as the reticulospinal tract contributes to recovery is unknown. Here, we examined the connectivity in these pathways to motor neurons after recovery from corticospinal lesions. Extensive unilateral lesions of the medullary corticospinal fibres in the pyramidal tract were made in three adult macaque monkeys. After an initial contralateral flaccid paralysis, motor function rapidly recovered, after which all animals were capable of climbing and supporting their weight by gripping the cage bars with the contralesional hand. In one animal where experimental testing was carried out, there was (as expected) no recovery of fine independent finger movements. Around 6 months post-lesion, intracellular recordings were made from 167 motor neurons innervating hand and forearm muscles. Synaptic responses evoked by stimulating the unlesioned ipsilateral pyramidal tract and the medial longitudinal fasciculus were recorded and compared with control responses in 207 motor neurons from six unlesioned animals. Input from the ipsilateral pyramidal tract was rare and weak in both lesioned and control animals, suggesting a limited role for this pathway in functional recovery. In contrast, mono- and disynaptic excitatory post-synaptic potentials elicited from the medial longitudinal fasciculus significantly increased in average size after recovery, but only in motor neurons innervating forearm flexor and intrinsic hand muscles, not in forearm extensor motor neurons. We conclude that reticulospinal systems sub-serve some of the functional recovery after corticospinal lesions. The imbalanced strengthening of connections to flexor, but not extensor, motor neurons mirrors the extensor weakness and flexor spasm which in neurological experience is a common limitation to recovery in stroke survivors.
Although a major descending motor pathway in mammals, the reticulospinal tract’s contribution to upper limb control in primates has received relatively little attention. Reticulospinal connections are widely assumed to be responsible for coordinated gross movements primarily of proximal muscles, whereas the corticospinal tract mediates fine movements, particularly of the hand. In this study, we employed intracellular recording in anaesthetised monkeys to examine the synaptic connections between the reticulospinal tract and antidromically identified cervical ventral horn motoneurons, focussing in particular on motoneurons projecting distally to wrist and digit muscles. We found that motoneurons receive mono- and disynaptic reticulospinal inputs, including monosynaptic excitatory connections to motoneurons that innervate intrinsic hand muscles, a connection not previously known to exist. We show that excitatory reticulomotoneuronal connections are as common and as strong in hand motoneuron groups as in forearm or upper arm motoneurons. These data suggest that the primate reticulospinal system may form a parallel pathway to distal muscles, alongside the corticospinal tract. Reticulospinal neurons are therefore in a position to influence upper limb muscle activity after damage to the corticospinal system as may occur in stroke or spinal cord injury, and may be a target site for therapeutic interventions.
SUMMARY1. The properties of interneurones located in the 4th lumbar segment of the cat spinal cord (L4 interneurones) have been investigated by intracellular and extracellular recording from individual neurones. The study focused on interneurones projecting to hind-limb motor nuclei and/or interposed in pathways from group II muscle afferents. The projection to motor nuclei was assessed from antidromic activation of the neurones by stimuli applied in the motor nuclei of the 7th lumbar (L7) segment.2. Interneurones which projected to gastrocnemius-soleus or hamstring motor nuclei were found in laminae VI and VII and at the border between laminae VII and VIII. The dominant peripheral input to most of them was from group II muscle afferents, but they were also influenced by group I muscle afferents and by afferents in cutaneous, joint and interosseous nerves. Both excitatory post-synaptic potentials (e.p.s.p.s) and inhibitory post-synaptic potentials (i.p.s.p.s) were evoked from all of these fibre systems.3. The same kind of multimodal input was also found in other interneurones in laminae VI and VII. However, their axonal projections were not identified and they might have included neurones projecting to motor nuclei (though outside the areas which were stimulated) as well as neurones with more local actions.4. Interneurones located in laminae IV and V of the dorsal horn appeared to constitute a separate functional population since both their projections and their input differed from those of the more ventrally located interneurones; none of the dorsal horn interneurones were found to project to motor nuclei and none had input from group I afferents, although they were influenced by group II muscle afferents and by afferents in cutaneous, joint and interosseous nerves.5. Many of the excitatory actions from group I and II afferents upon L4 interneurones were found to be evoked monosynaptically. A high proportion of L4 neurones synapsing upon motoneurones would thus be interposed in disynaptic reflex pathways from these afferents. In comparison to actions evoked via interneurones of the caudal lumbar segments, any post-synaptic potentials (p.s.p.s) * Present address:
SUMMARY1. The responses evoked by non-invasive electromagnetic and surface anodal electrical stimulation of the scalp (scalp stimulation) have been studied in the monkey. Conventional recording and stimulating electrodes, placed in the corticospinal pathway in the hand area of the left motor cortex, left medullary pyramid and the right spinal dorsolateral funiculus (DLF), allowed comparison of the actions of non-invasive stimuli and conventional electrical stimulation.2. Responses to electromagnetic stimulation (with the coil tangential to the skull) were studied in four anaesthetized monkeys. In each case short-latency descending volleys were recorded in the contralateral DLF at threshold. In two animals later responses were also seen at higher stimulus intensities. Both early and late responses were of corticospinal origin since they could be completely collided by appropriately timed stimulation of the pyramidal tract. The latency of the early response in the DLF indicated that it resulted from direct activation of corticospinal neurones: its latency was the same as the latency of the antidromic action potentials evoked in the motor cortex from the recording site in the DLF.3. Scalp stimulation, which was also investigated in three of the monkeys, evoked short-latency volleys at threshold and at higher stimulus intensities these were followed by later waves. The short-latency volleys could be collided from the pyramid and, at threshold, had latencies compatible with direct activation of corticospinal neurones. The longer latency volleys were also identified as corticospinal in origin.4. The latency of the early volley evoked by electromagnetic stimulation remained constant with increasing stimulus intensities. In contrast, with scalp stimulation above threshold the latency of the early volleys decreased considerably, indicating remote activation of the corticospinal pathway below the level of the motor cortex. In two monkeys both collision and latency data suggest activation of the corticospinal pathway as far caudal as the medulla.5. The majority of fast corticospinal fibres could be excited by scalp stimulation with intensities of 20% of maximum stimulator output. Electromagnetic MS 8118 S. A. EDGLEY AND OTHERS stimulation at maximum stimulator output elicited a volley of between 70 and 90 % of the size of the maximal volley evoked from the pyramidal electrodes.6. Electromagnetic stimulation was also investigated in one awake monkey during the performance of a precision grip task. Short-latency EMG responses were evoked in hand and forearm muscles. The onsets of these responses were approximately 0-8 ms longer than the responses evoked by electrical stimulation of the pyramid. Furthermore, they were comparable in latency to the fastest post-spike facilitation produced in the same muscles by identified cortico-motoneuronal cells.7. It is concluded that in the monkey, both electromagnetic and scalp stimulation of the motor cortex can activate corticospinal neurones directly, but that suprathreshold scalp stim...
SUMMARY1. A powerful projection from group II muscle afferents of hind-limb muscles to the 3rd, 4th and 5th segments of the lumbar spinal cord has been demonstrated by focal synaptic field potential recording.2. Field potentials were found at two locations: one in the dorsal horn (Rexed's laminae IV and V) and the other in the intermediate zone and ventral horn (Rexed's laminae VII and VIII). In the dorsal horn the field potentials were exceptionally large and were evoked only by group II afferents. At more ventral locations, they were smaller and were sometimes preceded by small field potentials evoked by group I afferents.3. At both locations field potentials could be evoked by stimulation of a number of hind-limb muscle nerves at strengths sufficient to activate group II afferents. However, some nerves consistently evoked more powerful effects than others and the largest potentials were from the nerves to quadriceps, sartorius and to the pretibial flexor muscles (tibialis anterior and extensor digitorum longus). Activation of articular afferents (from the knee joint nerve) or Pacinian corpuscle afferents (from the interosseous nerve) evoked small field potentials at some locations.4. In the dorsal horn the latency of the field potentials was so short that they must have been generated monosynaptically. Field potentials in the ventral horn had longer latencies, by 05-t10 ms, but they also appear to have been monosynaptically evoked by slowly conducting intraspinal collaterals. This conclusion is based primarily on the effects of intraspinal stimulation which was found to antidromically activate afferents with the appropriate latencies and thresholds.5. Evidence is presented that the dorsal and ventral field potentials are generated by afferents whose receptors can be activated by small (less than 100 /sm) muscle stretches.
In this review, the authors discuss some recent findings that bear on the issue of recovery of function after corticospinal tract lesions. Conventionally the corticospinal tract is considered to be a crossed pathway, in keeping with the clinical findings that damage to one hemisphere, for example, in stroke, leads to a contralateral paresis and, if the lesion is large, a paralysis. However, there has been great interest in the possibility of compensatory recovery of function using the undamaged hemisphere. There are several substrates for this including ipsilaterally descending corticospinal fibers and bilaterally operating neuronal networks. Recent studies provide important evidence bearing on both of these issues. In particular, they reveal networks of neurons interconnecting two sides of the gray matter at both brainstem and spinal levels, as well as intrahemispheric transcallosal connections. These may form "detour circuits" for recovery of function, and here the authors will consider some possibilities for exploiting these networks for motor control, even though their analysis is still at an early stage.
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