Task-related changes in propriospinal excitation from hand muscles to human flexor carpi radialis motoneurones

This study addresses whether there is excitation from human hand muscles to flexor carpi radialis (FCR) motoneurones mediated through propriospinal circuits and, if so, whether it is used in specific motor tasks. Electrical stimuli to the ulnar nerve at wrist level produced an excitation in FCR motoneurones with characteristics typical of a propriospinally mediated effect: low threshold (0.6 × motor threshold (MT)), a group I effect that was not reproduced by purely cutaneous stimuli, long central delay (4.1 ± 0.4 ms in single units), suppression when the stimulus intensity was increased, and facilitation of the corticospinal excitation at the premotoneuronal level. Ulnar-induced propriospinally mediated excitation was compared during selective voluntary contractions of the FCR and, at equivalent level of FCR EMG, during tasks in which the FCR was activated automatically in postural contractions rather than voluntarily (grip, pinching and pointing). The excitation was significantly greater during grip (and pinching) than during voluntary FCR contractions and pointing, whether measured in single motor units or tonic EMG activity, or whether the response to motor cortex stimulation was assessed as the compound motor-evoked potential or the corticospinal peak in single units. The discrepancy between the tasks appeared with ulnar intensities above 0.8 × MT and was then present across a wide range of stimulus intensities. This suggests a reduction in the corticospinal control of 'feedback inhibitory interneurones' mediating peripheral inhibition to propriospinal neurones during grip and pinching. The resulting more effective background excitation of propriospinal neurones by the peripheral input from hand muscles could contribute to stabilizing the wrist during grip.     

Evidence for corticospinal excitation of presumed propriospinal neurones in man.

1. The possibility that stimulation of the motor cortex facilitates transmission in the pathway mediating non-monosynaptic ('propriospinal') excitation from low-threshold afferents to upper limb motoneurones was investigated. 2. Convergence between peripheral afferent volleys (from the ulnar or musculo-cutaneous nerve) and corticospinal volleys (evoked by magnetic stimulation of the motor cortex) was investigated using the spatial facilitation technique. Thus the effects of these volleys on the flexor carpi radialis H reflex were compared when applied separately and together. When cortical stimulation was optimal for the muscle from which the conditioning volley originated the facilitation of the reflex on combined stimulation was significantly larger than the algebraic sum of the effects of separate stimuli. 3. The extra facilitation on combined stimulation had all the characteristics of 'propriospinal' excitation (low threshold, long central delay, brief duration and depression when the afferent input was increased), and it is suggested that this reflects corticospinal excitation of 'propriospinal' neurones. 4. When varying the time interval between cortical and test stimulations, it was shown that extra facilitation on combined stimulation began 1 ms later than the onset of the control reflex facilitation. Assuming that the latter onset reflects the arrival of the monosynaptic corticospinal volley at the motoneurone pool, this 1 ms delay suggests a disynaptic pathway for the cortical excitation of motoneurones through 'propriospinal' neurones. 5. As at the onset of voluntary movement, the pattern of the cortical excitation of 'propriospinal' neurones was quite specific: extra facilitation of the reflex on combined stimulation only occurred when the cortical volley was preferentially directed to motoneurones supplying the muscle from which the afferents used for the peripheral volley originated. 6. It is concluded that corticospinal axons activate human 'propriospinal' neurones and thereby produce disynaptic excitation of the motoneurone pool. Given temporal summation with the monosynaptic excitation, this 'propriospinally mediated' disynaptic excitation might make a significant contribution to the evoked EMG potential.     

Handedness-related asymmetry in transmission in a system of human cervical premotoneurones

 The possibility was investigated that human handedness is associated with an asymmetrical cortical and/or peripheral control of the cervical premotoneurones (PreMNs) that have been shown to mediate part of the descending command to motoneurones of forearm muscles . Heteronymous facilitation evoked in the ongoing voluntary extensor carpi radialis (ECR) electromyographic activity (EMG) by weak (0.8 times motor threshold) stimulation of the musculo-cutaneous (MC) nerve was assessed during tonic co-contraction of biceps and ECR. Suppression evoked by stimulation of a cutaneous nerve (superficial radial, SR) at 4 times perception threshold in both the voluntary EMG and in the motor evoked potential (MEP) elicited in ECR by transcranial magnetic stimulation (TMS) was investigated during isolated ECR contraction. Measurements were performed within time windows or at interstimulus intervals where peripheral and cortical inputs may interact at the level of PreMNs. Results obtained on both sides were compared in consistent right- and left-handers. MC-induced facilitation of the voluntary ECR EMG was significantly larger on the preferred side, whereas there was no asymmetry in the SR-evoked depression of the ongoing ECR EMG. In addition, the suppression of the ECR MEP by the same SR stimulation was more pronounced on the dominant side during unilateral, but not during bilateral, ECR contraction. It is argued that (1) asymmetry in MC-induced facilitation of the voluntary EMG reflects a greater efficiency of the peripheral heteronymous volley in facilitating PreMNs on the dominant side; (2) asymmetry in SR-induced suppression of the MEP during unilateral ECR contraction, which is not paralleled by a similar asymmetry of voluntary EMG suppression, reflects a higher excitability of cortical neurones controlling inhibitory spinal pathways to cervical PreMNs on the preferred side. Received: 20 May 1998 / Accepted: 15 October 1998     

The nature of corticospinal paths driving human motoneurones during voluntary contractions

The properties of the human motor cortex can be studied non-invasively using transcranial magnetic stimulation (TMS). Stimulation at high intensity excites corticospinal cells with fast conducting axons that make direct connections to motoneurones of human upper limb muscles, while low-intensity stimulation can suppress ongoing EMG. To assess whether these cells are used in normal voluntary contractions, we used TMS at very low intensities to suppress the firing of single motor units in biceps brachii ( n = 14) and first dorsal interosseous (FDI, n = 6). Their discharge was recorded with intramuscular electrodes and cortical stimulation was delivered at multiple intensities at appropriate times during sustained voluntary firing at ∼10 Hz. For biceps, high-intensity stimulation produced facilitation at 17.1 ± 2.1 ms (lasting 2.4 ± 0.9 ms), while low-intensity stimulation (below motor threshold) produced suppression (without facilitation) at 20.2 ± 2.1 ms (lasting 7.6 ± 2.2 ms). For FDI, high-intensity stimulation produced facilitation at 23.3 ± 1.2 ms (lasting 1.8 ± 0.4 ms), with suppression produced by low-intensity stimulation at 25.2 ± 2.6 ms (lasting 7.5 ± 2.6 ms). The difference between the onsets of facilitation and suppression was short: 3.1 ± 1.2 ms for biceps and 2.0 ± 1.5 ms for FDI. This latency difference is much less than that previously reported using surface EMG recordings (∼10 ms). These data suggest that low-intensity cortical stimulation inhibits ongoing activity in fast-conducting corticospinal axons through an oligosynaptic (possibly disynaptic) path, and that this activity is normally contributing to drive the motoneurones during voluntary contractions.     

Modulation of motor cortex excitability by median nerve and digit stimulation

We investigated the time course of changes in motor cortex excitability after median nerve and digit stimulation. Although previous studies showed periods of increased and decreased corticospinal excitability following nerve stimulation, changes in cortical excitability beyond 200 ms after peripheral nerve stimulation have not been reported. Magnetoencephalographic studies have shown an increase in the 20-Hz rolandic rhythm from 200 to 1000 ms after median nerve stimulation. We tested the hypothesis that this increase is associated with reduced motor cortex excitability. The right or left median nerve was stimulated and transcranial magnetic stimulation (TMS) was applied to left motor cortex at different conditioning-test (C-T) intervals. Motor-evoked potentials (MEPs) were recorded from the right abductor pollicis brevis (APB), first dorsal interosseous (FDI), and extensor carpi radialis (ECR) muscles. Right median nerve stimulation reduced test MEP amplitude at C-T intervals from 400 to 1000 ms for APB, at C-T intervals from 200 to 1000 ms for FDI, and at C-T intervals of 200 and 600 ms for ECR, but had no effect on FDI F-wave amplitude at a C-T interval of 200 ms. Left median nerve (ipsilateral to TMS) stimulation resulted in less inhibition than right median nerve stimulation, but test MEP amplitude was significantly reduced at a C-T interval of 200 ms for all three muscles. Digit stimulation also reduced test MEP amplitude at C-T intervals of 200–600 ms. The time course for decreased motor cortex excitability following median nerve stimulation corresponds well to rebound of the 20-Hz cortical rhythm and supports the hypothesis that this increased power represents cortical deactivation. Received: 11 December 1998 / Accepted: 30 April 1999     

Integration in descending motor pathways controlling the forelimb in the cat

Summary A previously described disynaptic pathway from cortex to forelimb motoneurones whose intercalated neurones were excited both from other descending pathways and from forelimb afferents (Illert et al., 1976a, b) has been further analysed, mainly with respect to the location of the relay cells and their axons.Disynaptic EPSPs evoked in forelimb motoneurones by stimulation of the pyramid remained after complete transection of the corticospinal tract in C5 rostral to the forelimb segments but were abolished after a more rostral transection of the tract in the C2 segment. Corresponding findings were made with disynaptic rubral EPSPs after transection of the rubrospinal tract in these segments. It is concluded that disynaptic cortico-motoneuronal and rubro-motoneuronal excitation is relayed by propriospinal neurones originating in the C3–C4 segments. Other lesion experiments revealed that the axons of these propriospinal neurones descend to forelimb motoneurones in the ventrolateral part of the lateral funicle.Spatial facilitation of transmission from the corticospinal and rubrospinal tracts after transection of them in C5 occurred with a time course showing monosynaptic convergence from these pathways on common propriospinal neurones.Facilitation of disynaptic pyramidal EPSPs from the dorsal tegmentum remained after transection of the corticospinal tract at C5 but was abolished after a transection at C2. It is postulated that corticospinal and presumed tectospinal fibres converge onto common neurones in the propriospinal relay but evidence is also given for a more rostral relay (probably bulbar) with a similar convergence.The oligo- (probably mono-)synaptic facilitation of the disynaptic pyramidal EPSP evoked by volleys in cutaneous and group I muscle afferents from the forelimb likewise remained after a C5 transection of the corticospinal tract but was abolished after an additional C5 lesion in the dorsal column. It is concluded that propriospinal relay cells receive excitatory action from forelimb afferents ascending in the dorsal column. Spatial facilitation experiments using three tests revealed that propriospinal neurones monosynaptically excited from both corticospinal and rubrospinal fibres also receive excitation from cutaneous forelimb afferents.It is postulated that the propriospinal relay provides an important route for fast activation of forelimb motoneurones from the brain. The convergent monosynaptic excitation from several important motor centres in the brain is considered in relation to the general problem of the functional relationship between higher motor centres. The convergent action from forelimb afferents is taken to suggest that a descending command for a forelimb movement can be modified from the forelimb while on its way to the motoneurones.Supported by the Deutsche Forschungsgemeinschaft     

Pyramidal actions in identified radial motornuclei of the cat

This study aimed to establish the projection from the corticospinal tract (CST) to the motoneurones innervating the deep radial (DR) forelimb muscles. In the anaesthetized cat stimulation of the contralateral pyramid and intracellular recording from identified forelimb motoneurones was used. A train of pyramidal stimuli evoked disynaptic EPSPs in DR motoneurones. The effects were very similar in the different nuclei. Pyramidal IPSPs had a slightly longer latency and occurred in most cases together with disynaptic EPSPs. It is suggested that the inhibitory actions to the distal forelimb are predominantly relayed in a trisynaptic pathway, but that a disynaptic linkage seems possible as well. The disynaptic pyramidal EPSPs remained after CST transection in C5. They were abolished after CST transections in C2. It is concluded that disynaptic corticospinal excitation of distal DR motornuclei is relayed in a short midcervical propriospinal system. Transection experiments at different cervical levels suggest that the majority of the propriospinal neurones is located in C3-C4. The CST facilitated a variety of reflex pathways to motoneurones innervating distal forelimb muscles. Disynaptic excitatory and inhibitory effects from cutaneous and low threshold group I muscle afferents were common. They were present in all investigated nuclei and powerfully facilitated from the CST. It is suggested that this allows the brain to adapt the reflex mechanisms of the distal forelimb to the synergistic-antagonistic relations between the muscles, which are changing according to the performed movement.     

Pattern of projections of group I afferents from forearm muscles to motoneurones supplying biceps and triceps muscles in man

Summary (1) Two independent methods were used, in man, to assess the modifications of the excitability of biceps and triceps brachii motoneurone pools following the stimulation of group I afferents coming from muscles acting at the wrist: (a) the modifications of the excitability of a motoneuronal population were studied using a reflex technique, (b) the modifications of the excitability of an isolated motor unit were estimated using a post-stimulus time histogram (p.s.t.h.) method. (2) The activation of group I afferents contained in the median nerve, originating from wrist flexors and pronators, resulted in a strong, short-latency facilitation of the biceps brachii motoneurones. A similar effect was also evoked by stimulation of group I afferents in the radial nerve, distally to the branch supplying the brachio-radialis muscle. The latency of both median and radial-induced facilitations is compatible with a monosynaptic linkage. (3) The stimulation of group I afferents in the median or the radial nerves produced inhibition of triceps motoneurones, with a latency compatible with a disynaptic linkage. (4) The prolonged vibration of the tendon of the flexor carpi radialis (FCR) or of the extensor carpi radialis (ECR) raised the threshold for both the facilitation of biceps and the inhibition of triceps motoneurones. The same pattern of excitatory and inhibitory convergence could also be obtained when the electrical conditioning stimulus to the median or radial nerves was replaced by a tap applied to the tendons of FCR or ECR respectively. Both results suggest that the conditioning fibres were Ia fibres. (5) The pattern of distribution of Ia afferents from muscles acting at the wrist onto motoneurones of muscles acting at the elbow has been compared to that described in the cat and monkey. A comparison has also been made between Ia connections of muscles acting at different joints in the upper and lower limb in man. The differences are discussed in relation to the manipulating capacity of the hand.     

Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey.

1. The neuronal mechanism of disynaptic inhibition of spinal motoneurones by the corticospinal tract was investigated in Macaca irus. Surface stimulation or weak intracortical stimulation was used in order to evoke the inhibition. Intracellular records were taken from motoneurones in lumbar segments. 2. Both the disynaptic i.p.s.p.s evoked from group Ia afferents and the disynaptic i.p.s.p.s evoked from corticospinal fibres were found to be depressed by conditioning stimulation of motor axons to antagonistic muscles. Mutual facilitation of the actions from these two fibre systems occurred when nerve impulses set up in them reached the explored spinal segment synchronously. These observations led to the conclusion that disynaptic i.p.s.p.s from group Ia afferents and from the motor cortex are mediated by common interneurones. 3. No evidence either for or against projections of the same pyramidal tract cells to motoneurones of one motor nucleus and to interneurones interposed between group Ia afferents and motoneurones of an antagonistic muscle could be obtained by comparing cortical areas from which monosynaptic e.p.s.p.s and disynaptic i.p.s.p.s were evoked in the different motor nuclei. 4. The areas from which the disynaptic i.p.s.p.s were evoked in individual motoneurones appeared to be similar in size to the areas of cortical monosynaptic projections to motoneurones and showed similar degrees of overlap, indicating that the projections of pyramidal tract cells to Ia inhibitory interneurones are as extensive as to motoneurones and that they are similarly organized.     

Cortical excitability and motor task in man: an investigation of the wrist extensor motor area

Task-related changes in the corticospinal excitation of the right extensor carpi radialis (ECR) muscle were investigated in 16 healthy human subjects. The subjects were asked to perform a tonic isometric wrist extension or to clench their hand around a manipulandum, thereby coactivating the antagonistic wrist muscles. At matched levels of background EMG in the ECR muscle, transcranial magnetic stimulation (TMS) was applied through a figure-of-eight coil at 20-30 sites spaced 1 cm apart over the hand area of the left motor cortex. The cortical maps of the representation of the ECR muscle constructed in this way did not change between the two motor tasks. Nevertheless, for all investigated cortical sites TMS evoked a smaller motor evoked potential (MEP) in the ECR muscles during hand clenching than during wrist extension. A similar decrease in the short-latency peak in the poststimulus time histogram (PSTH) of single ECR motor units to TMS during hand clenching was found in seven subjects (number of motor units = 35). In contrast, short-latency peaks in the PSTH evoked by electrical stimulation of the motor cortex had a similar size during the two tasks (number of motor units = 9; two subjects). Already the initial 0.5-1.0 ms of the short-latency peak evoked by TMS was depressed during hand clenching, which suggests that decreased excitability of corticospinal cells with monosynaptic projections onto ECR motor units was involved. This decreased excitability was not explained by increased intracortical inhibition, which was found to be of a similar size during hand clenching and wrist extension. The task-related changes in the efficiency of the motor cortex output are discussed in relation to the function of the wrist antagonist muscles in handling and gripping tasks.     

Origin of facilitation of motor-evoked potentials after paired magnetic stimulation: direct recording of epidural activity in conscious humans

A magnetic transcranial conditioning stimulus given over the motor cortex at intensities below active threshold for obtaining motor-evoked potentials (MEPs) facilitates EMG responses evoked at rest in hand muscles by a suprathreshold magnetic stimulus given 10-25 ms later. This is known as intracortical facilitation (ICF). We recorded descending volleys produced by single and paired magnetic motor cortex stimulation through high cervical epidural electrodes implanted for pain relief in six conscious patients. At interstimulus intervals (ISIs) of 10 and 15 ms, although MEP was facilitated, there was no change in the amplitude or number of descending volleys. An additional I wave sometimes was observed at 25 ms ISI. In one subject, we also evaluated the effects of reversing the direction of the induced current in the brain. At 10 ms ISI, the facilitation of the MEPs disappeared and was replaced by slight suppression; at 2 ms ISI, there was a pronounced facilitation of epidural volleys. Subsequent experiments on healthy subjects showed that a conditioning stimulus capable of producing ICF of MEPs had no effect on the EMG response evoked by transmastoidal electrical stimulation of corticospinal tract. We conclude that ICF occurs because either 1) the conditioning stimulus has a (thus far undetected) effect on spinal cord excitability that increases its response to the same amplitude test volley or 2) that it can alter the composition (but not the amplitude) of the descending volleys set up by the test stimulus such that a larger proportion of the activity is destined for the target muscle.     

Interaction of transcranial magnetic stimulation and electrical transmastoid stimulation in human subjects

Transcranial magnetic stimulation activates corticospinal neurones directly and transsynaptically and hence, activates motoneurones and results in a response in the muscle. Transmastoid stimulation results in a similar muscle response through activation of axons in the spinal cord. This study was designed to determine whether the two stimuli activate the same descending axons. Responses to transcranial magnetic stimuli paired with electrical transmastoid stimuli were examined in biceps brachii in human subjects. Twelve interstimulus intervals (ISIs) from −6 ms (magnet before transmastoid) to 5 ms were investigated. When responses to the individual stimuli were set at 10-15 % of the maximal M-wave, responses to the paired stimuli were larger than expected at ISIs of −6 and −5 ms but were reduced in size at ISIs of −2 to 1 ms and at 3 to 5 ms. With individual responses of 3-5 % of maximal M-wave, facilitation still occurred at ISIs of −6 and −5 ms and depression of the paired response at ISIs of 0, 1, 4 and 5 ms. The interaction of the response to transmastoid stimulation with the multiple descending volleys elicited by magnetic stimulation of the cortex is complex. However, depression of the response to the paired stimuli at short ISIs is consistent with an occlusive interaction in which an antidromic volley evoked by the transmastoid stimulus collides with and annihilates descending action potentials evoked by the transcranial magnetic stimulus. Thus, it is consistent with the two stimuli activating some of the same corticospinal axons.     

The excitability of human cortical inhibitory circuits responsible for the muscle silent period after transcranial brain stimulation

The silent period after transcranial magnetic brain stimulation mainly reflects the activity of inhibitory circuits in the human motor cortex. To assess the excitability of the cortical inhibitory mechanisms responsible for the silent period after transcranial stimulation, we studied, in 15 healthy human subjects, the recovery cycle of the silent period evoked by transcranial and mixed nerve stimulation delivered with a paired stimulation technique. The recovery cycle is defined as the time course of the changes in the size or duration of a conditioned test response when pairs of stimuli (conditioning and test) are used at different conditioning-test intervals. The recovery cycle of the duration of the silent period in the first dorsal interosseous (FDI) muscle during maximum voluntary contraction after transcranial magnetic stimulation was studied by delivering paired magnetic shocks (a conditioning shock and a test shock) at 120% motor-threshold intensity. Conditioning-test intervals ranged from 20-550 ms. The recovery cycle of the silent period in the FDI muscle during maximum voluntary contraction after nerve stimulation was evaluated by paired, supramaximum bipolar electrical stimulation of the ulnar nerve at the wrist (conditioning-test intervals ranging from 20 to 550 ms). Electromyographic activity was recorded by a pair of surface-disk electrodes over the FDI muscle. The recovery cycle of the silent period after transcranial magnetic stimulation delivered through the large round coil showed two phases of facilitation (lengthening of the silent period), one at 20-40 ms and the other at 180-350 ms conditioning-test intervals, with an interposed phase of inhibition (shortening of the silent period) at 80-160 ms. The conditioning magnetic shock left the size of the test motor-evoked potentials statistically unchanged during maximum voluntary contraction. Paired transcranial stimulation with a figure-of-eight coil increased the duration of the test silent period only at short conditioning-test intervals. Conditioning nerve stimulation left the silent period produced by test nerve stimulation unchanged. In conclusion, after a single transcranial magnetic shock, inhibitory circuits in the human motor cortex undergo distinctive short-term changes in their excitability, probably involving different mechanisms.     

Origin of corticospinal neurones evoking disynaptic excitation in forelimb motoneurones mediated via C3-C4 propriospinal neurones in the cat

Intracellular recording was made from forelimb motoneurones in the cat (alpha-chloralose anaesthesia) during electrical stimulation of corticospinal neurones (CSNs) and their afferents in the contralateral cortex. Axons of the CSNs were stimulated in the contralateral pyramid. The corticospinal tract was transected at the C5/C6 segmental border in order to restrict transmission through the C3-C4 propriospinal neurones (C3-C4 PNs). Di- and trisynaptic cortical EPSPs could be evoked after transection of the corticospinal fibres in C5/C6 but not after a corresponding transection in C2/C3. Pyramidal stimulation elicited disynaptic EPSPs that were abolished after a C2/C3 transection. Disynaptic pyramidal EPSPs, mediated via C3-C4 propriospinal neurones could be facilitated by a single cortical stimulation. It is concluded that di- and trisynaptic cortical EPSPs and disynaptic pyramidal EPSPs are mediated via the same C3-C4 PNs. Cortical surface stimulation showed that di- and trisynaptic cortical EPSPs could be evoked from distinct spots in the lateral part of the anterior sigmoid gyrus (Sig. a) and/or in the rostral part of the lateral sigmoid gyrus (Sig. l). No cortical EPSPs or facilitation of pyramidal disynaptic EPSPs was evoked from the posterior part of the Sig. l, posterior sigmoid gyrus, coronal gyrus, lateral gyrus, suprasylvian gyrus and ectosylvian gyrus. It is concluded that the CSNs, which issue the command for visually guided target reaching with the forelimb via the C3-C4 PNs, originate in the lateral part of the Sig. a and in the rostral part of the Sig. l. A dual representation of the forelimb in the primary motor cortex of the cat has previously been proposed. The present results show that with respect to one identified interneuronal system like the C3-C4 propriospinal system, the CSNs may have their origin restricted to one region of the primary motor cortex.     

Medium-latency reflex response elicited from the flexor carpi radialis by radial nerve stimulation

The H reflex obtained from the flexor carpi radialis muscle by median nerve stimulation is a well-known monosynaptic reflex. However, the origin of the late responses is still contentious. Radial nerve stimulation was performed through the spiral groove, and EMG recording was obtained from the flexor carpi radialis (FCR) and extensor carpi radialis (ECR) muscles. An M response followed by an F response was achieved from the ECR by radial nerve stimulation; the antagonistic FCR muscle elicited a late response. A total of 25 cases were included in this study. In 22 of these cases, a response with a latency of 40.97 ± 5.35 ms was obtained from the FCR by radial nerve stimulation. When extension of the hand was restricted, the response disappeared in five of nine cases. Application of cold markedly suppressed the response and prolonged the latency of the FCR medium-latency reflex response (FCR-MLR). Oral tizanidine considerably suppressed the FCR-MLR response. Two out of eight cases did not exhibit any response. No response could be recorded from a patient with complete amputation of the right hand. The FCR-MLR is the reflex caused by stretching of the FCR muscle from radial nerve stimulation, and it is greatly influenced by group II afferents.     

Convergence of skin reflex and corticospinal effects in segmental and propriospinal pathways to forelimb motoneurones in the cat

The organization of facilitatory convergence from cutaneous afferents (Skin) and the corticospinal tract (pyramidal tract, Pyr) in pathways to forelimb motoneurones of mainly distal muscles was studied in anaesthetized cats by analysing postsynaptic potentials (PSPs), which were spatially facilitated by combinations of stimuli to the two sources at different time intervals. Conditioning Pyr volleys facilitated Skin-evoked PSPs of fixed (1.2–3.6 ms) central latencies (Skin PSPs), suggesting that disynaptic and polysynaptic skin reflex pathways are facilitated from the pyramidal tract. The shortest latencies (1.2–1.7 ms) of pyramidal facilitation suggested direct connection of pyramidal fibres with last order neurones of skin reflex pathways. Conditioning Skin volleys facilitated Pyr-evoked PSPs of fixed, mostly disynaptic latencies (1.0–2.5 ms; Pyr PSPs), suggesting that pyramido-motoneuronal pathways are facilitated from Skin at a premotoneuronal level. The shortest pathway from skin afferents to the premotor neurones appeared to be monosynaptic. Although Pyr and Skin volleys were mutually facilitating, the facilitation curve of Pyr PSPs and that of Skin PSPs were discontinuous to each other, with the peak facilitation at different Skin-Pyr volley intervals. Transection of the dorsal column (DC) at the C5/C6 border had little effect on the latencies or amplitudes evoked by maximal stimulation and the pyramidal facilitation of Skin PSPs. In contrast, the facilitation of Pyr PSPs by Skin stimulation was greatly decreased after the DC transection, and the facilitation curve of Pyr PSPs was continuous to that of Skin PSPs, with no separate peak. Latencies of Pyr PSPs ranged similarly to those in DC intact preparations. More rostral DC transection (C4/C5 border) reduced Skin-facilitated Pyr excitatory PSPs (EPSPs) less than C5/C6 lesions, suggesting that the C5 segment also contains neurones mediating Skin-facilitated Pyr EPSPs. The results show that convergence from skin afferents and the corticospinal tract occurs at premotor pathways of different cervical segments. We suggest that corticospinal facilitation of skin reflex occurs mostly in the brachial segments and Skin facilitation of cortico-motoneuronal effects takes place largely in the rostral cervical segments and partly in the brachial segments.     

Origin of corticospinal neurones evoking monosynaptic excitation in C3--C4 propriospinal neurones in the cat

Intracellular recording was made from propriospinal neurones (PNs) in the C3-C4 spinal cord segments in the cat (alpha-chloralose anaesthesia). The effect of electrical stimulation of corticospinal neurones (CSNs) in the cortex was investigated. Short C3-C4 PNs were identified by antidromic activation of their axons in the ventral horn in C6/C7 and in the lateral reticular nucleus. Long PNs were antidromically identified from Th12-13. In short PNs, monosynaptic excitory postsynoptic potentials (EPSPs) were elicited from the rostral part of the lateral sigmoid gyrus, the lateral part of the anterior sigmoid gyrus in area 4 gamma and in the adjacent area 6. Two subtypes of short PNs were identified. PNs of type I received monosynaptic EPSPs from the rostral part of the lateral sigmoid gyrus, the lateral part of the anterior sigmoid gyrus in area 4 gamma, which is from the same region as disynaptic cortical EPSPs were evoked in forelimb motoneurones. PNs of type II received monosynaptic EPSPs from regions slightly more rostrally in the anterior sigmoid gyrus in area 4 gamma and in the adjacent area 6, which is outside the region from which disynaptic EPSPs could be evoked in forelimb motoneurones. Long PNs received monosynaptic EPSPs, like the short PNs, by stimulation in the rostral part of the lateral sigmoid gyrus, the lateral part of the anterior sigmoid gyrus in area 4 gamma and in the adjacent area 6. In contrast, the long PNs also received monosynaptic EPSPs from area 3b near the border of area 1. The present results show segregation of the cortical control to functionally different premotoneuronal systems and suggest that this control could in part be separated for subtypes of short C3-C4 PNs.     

Long-loop reflex from arm afferents to remote muscles in normal man

The present study was designed to examine the effects of median nerve stimulation on motoneurones of remote muscles in healthy subjects using H-reflex, averaged EMG and PSTH methods. Stimulation of the median nerve induced facilitation of soleus H-reflex from about 50 ms and it reached a peak at about 100 ms of conditioning-test interval. Afferents that induced the facilitation consisted of at least two types of fibres, the high-threshold cutaneous fibres and the low-threshold fibres. When the effects were examined by the averaged surface EMG and PSTH, no facilitation but rather inhibition or inhibition-facilitation was induced in all tested muscles except for the upper limb muscles on the stimulated side. The inhibition latency was shortest in masseter muscle and longest in leg muscles, while values for the contralateral upper limb muscles were in the middle, indicating that the onset of inhibition was delayed from rostral to caudal muscles. Inputs from the median nerve converged to inhibitory interneurones, which mediate the masseter inhibitory reflex. Our findings suggested that inputs from the median nerve initially ascend to the brain, at least to the brainstem, and then descend to the spinal cord. Therefore, inhibition induced by median nerve stimulation was not considered as an interlimb reflex mediated by a propriospinal pathway, but long-loop reflex, at least via the pons. The discrepancy between the results of reflex and motor units suggests that facilitation of soleus H-reflex following median nerve stimulation was mainly due to reduced presynaptic inhibition.     

On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects

Non-invasive transcranial magnetic stimulation (TMS) of motor cortex induces motor evoked potentials in contralateral muscles which are thought to be conducted by the corticospinal tract. Furthermore, inhibitory actions can be elicited by TMS which appear directly after the motor evoked potential (postexcitatory inhibition, PI) and can be visualized by blockade of tonic voluntary EMG activity. It was the aim of the present study to answer the questions of whether this inhibitory action is mainly of cortical or of spinal origin, which brain area generates this inhibition, and whether the duration of PI differs between proximal and distal muscles. Experiments were performed on a total of 34 healthy volunteers. Brain stimuli were delivered with a Novametrix Magstim 200HP with a maximum output of 2.0 T, and stimulation was performed during tonic voluntary activation of the muscle under study. Stimulation strength was 1.5 times threshold level. Duration of PI was defined as the time from the onset of the motor evoked potential to the reoccurrence of the EMG background activity. PI was found more pronounced in distal hand muscles than in proximal arm and leg muscles. The largest PI values were observed when the primary motor cortex was stimulated. To test the excitability of the spinal motoneurones during PI, cortical double stimulation at various intervals was performed and the soleus H-reflex was evoked at different intervals after cortical stimulation. Neither test revealed a decrease in the excitability of the spinal motoneurones during PI. These findings imply that spinal segmental inhibitory action cannot account for PI and that, most probably, inhibitory actions within the motor cortex play a major role in the genesis of PI.Dedicated to the memory of Prof. Dr. O. Creutzfeldt     

Integration in descending motor pathways controlling the forelimb in the cat

Summary Effects of stimulation in the medullary reticular formation (RF) on C3-C4 propriospinal neurones (PNs) were investigated in two series of experiments: (1) indirectly by analyzing how propriospinal transmission to forelimb motoneurones is modified by reticular stimuli; (2) directly by intracellular recording from C3-C4 neurones, which were identified as propriospinal by their antidromic activation from the C6 segment.Propriospinally mediated disynaptic EPSPs evoked in motoneurones from the pyramid (Pyr) and the red nucleus (NR) were effectively facilitated by conditioning stimulation in the RF with a time course of facilitation indicating monosynaptic linkage to the PNs. Propriospinally mediated trisynaptic IPSPs were facilitated less regularly and sometimes instead depressed by conditioning stimulation in the RF. The depression is at least partly due to inhibition of the first order PNs.Recording from C3-C4 PNs revealed that many of them were excited or inhibited by single stimuli in the RF. The brief latency of the EPSPs evoked in these neurones shows monosynaptic linkage from fast reticulospinal fibres. Some IPSPs were similarly monosynaptically evoked from fast fibres and observations are presented suggesting that longer latency IPSPs are monosynaptically mediated by slower fibres. Facilitation of propriospinal transmission to motoneurones as well as the EPSPs and IPSPs in PNs were evoked from a region within or close to the nucleus reticularis gigantocellularis.Convergence of monosynaptic EPSPs from Pyr, NR, tectum, and RF was common in C3-C4 PNs. Linear summation of the EPSPs from RF with those evoked from cortico-, rubro-, or tectospinal tracts shows that the former are not due to stimulation of collaterals which the latter tracts may have in RF. Mediation of the EPSPs and IPSPs by descending, rather than by antidromically activated ascending fibres, was indicated by temporal facilitation produced by RF stimuli, subliminal for evoking monosynaptic PSPs in the PNs. Stimulation of the labyrinth did not evoke disynaptic PSPs in any of the PNs investigated.It is concluded that the C3-C4 PNs projecting to forelimb motoneurones can be excited not only from the cortico-, rubro-, and tectospinal tracts (Illert et al. 1977, 1978) but also by reticulospinal fibres.Abbreviations LF lateral funiculus - MLF medial longitudinal fasciculus - NR nucleus ruber - PNs propriospinal neurones - Pyr pyramids - T tectum - RF reticular formation - i ipsilateral - co contralateral - Bi biceps - Br brachialis - DR deep radial - Tri triceps This work was supported by the Swedish Medical Research Council (Project No. 94)