R. N. Lemon

Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation

1 Recordings were made of local field potential (slow waves) and pyramidal tract neurone (PTN) discharge from pairs of sites separated by a horizontal distance of up to 1.5 mm in the primary motor cortex of two conscious macaque monkeys performing a precision grip task. 2 In both monkeys, the slow wave recordings showed bursts of oscillations in the 20–30 Hz range. Spectral analysis revealed that the oscillations were coherent between the two simultaneously recorded cortical sites. In the monkey from which most data were recorded, the mean frequency of peak coherence was 23.4 Hz. 3 Coherence in this frequency range was also seen between cortical slow wave recordings and rectified EMG of hand and forearm muscles active during the task, and between pairs of rectified EMGs. 4 The dynamics of the coherence were investigated by analysing short, quasi‐stationary data segments aligned relative to task performance. This revealed that the 20–30 Hz coherent oscillations were present mainly during the hold phase of the precision grip task. 5 The spikes of identified PTNs were used to compile spike‐triggered averages of the slow wave recordings. Oscillations were seen in 11/17 averages of the slow wave recorded on the same electrode as the triggering spike, and 11/17 averages of the slow wave recorded on the distant electrode. The mean period of these oscillations was 45.8 ms. 6 It is concluded that oscillations in the range 20–30 Hz are present in monkey motor cortex, are coherent between spatially separated cortical sites, and encompass the pyramidal tract output neurones. They are discernable in the EMG of active muscles, and show a consistent task‐dependent modulation.

The role of synchrony and oscillations in the motor output

Abstract There is currently much interest in the synchronisation of neural discharge and the potential role it may play in information coding within the nervous system. We describe some recent results from investigations of synchronisation within the motor system. Local field potentials (LFPs) and identified pyramidal tract neurones (PTNs) were recorded from the primary motor cortex of monkeys trained to perform a precision grip task. The LFPs showed bursts of oscillatory activity at 20–30 Hz, which were coherent with the rectified electromyographs (EMG) of contralateral hand and forearm muscles. This oscillatory synchronisation showed a highly specific task dependence, being present only during the part of the task when the animal maintained a steady grip and not during the movement phases before or after it. PTNs were phase-locked to LFP oscillations, implying that at least part of the coherence between cortical activity and EMG was mediated by corticospinal fibres. The phase locking of the PTNs to LFP oscillations produced task-dependent oscillatory synchronisation between PTN pairs, as assessed by the single-unit cross-correlation histogram. Recordings were also made from normal human subjects performing a precision grip similar to that used in the monkey recordings. Pairs of EMGs recorded from intrinsic hand and forearm muscles showed 20–30 Hz coherence, which modulated during task performance, being present only during periods of steady contraction. We suggest that these changes in EMG-EMG synchronisation reflect changing levels of synchronous drive from the corticospinal system. The generation of oscillations in the cortex is discussed in the light of results from a model of local cortical circuits. Other modelling work has shown that synchrony in the corticospinal inputs could act to recruit motoneurones more efficiently, producing more output force from a muscle than asynchronous inputs firing at the same mean rate. A speculative hypothesis is presented on the role of synchronous oscillations in the motor system, which is consistent with experimental observations to date.

Task-dependent modulation of 15-30 Hz coherence between rectified EMGs from human hand and forearm muscles

1 Recent reports have shown task‐related changes in oscillatory activity in the 15‐30 Hz range in the sensorimotor cortex of human subjects and monkeys during skilled hand movements. In the monkey these oscillations have been shown to be coherent with oscillatory activity in the electromyographic activity of hand and forearm muscles. 2 In this study we investigated the modulation of oscillations in the electromyogram (EMG) of human volunteers during tasks requiring precision grip of two spring‐loaded levers. 3 Two tasks were investigated: in the ‘hold’ task, subjects were required to maintain a steady grip force (ca 2·1 N or 2·6 N) for 8 s. In the ‘ramp’ task, there was an initial hold period for 3 s (force ca 2·1 N) followed by a linear increase in grip force over a 2 s period. The task ended with a further steady hold for 3 s at the higher force level (ca 2·6 N). 4 Surface EMGs were recorded from five hand and forearm muscles in 12 subjects. The coherence of oscillatory activity was calculated between each muscle pair. Frequencies between 1 and 100 Hz were analysed. 5 Each subject showed a peak in the coherence spectra in the 15‐30 Hz bandwidth during the hold task. This coherence was absent during the initial movement of the levers. During the ramp task the coherence in the 15‐30 Hz range was also significantly reduced during the movement phase, and significantly increased during the second hold period, relative to the initial hold. 6 There was coherence between the simultaneously recorded magnetoencephalogram (MEG) and EMG during steady grip in the hold task; this coherence disappeared during the initial lever movement. Using a single equivalent current dipole source model, the coherent cortical activity was localized to the hand region of the contralateral motor cortex. This suggests that the EMG‐EMG coherence was, therefore, at least in part, of cortical origin. 7 The results are discussed in terms of a possible role for synchrony in the efficient recruitment of motor units during maintained grip.

Does a C3-C4 propriospinal system transmit corticospinal excitation in the primate? An investigation in the macaque monkey.

1 Synaptic responses to electrical stimulation of the contralateral pyramidal tract were measured in intracellular recordings from 206 upper limb motoneurones in ten chloralose‐anaesthetized macaque monkeys. The objective was to search for evidence of a disynaptic excitatory pathway via C3‐C4 propriospinal interneurones similar to that in the cat. 2 In monkeys with intact spinal cords, only a small proportion of motoneurones (19 %) responded with late EPSPs to repetitive stimulation of the pyramid; only 3 % had segmental latencies that were appropriate for a disynaptic pathway. 3 From previous studies in the cat, it was expected that a lesion to the dorsolateral funiculus (DLF) at C5 would interrupt the corticospinal input to the spinal segments supplying upper limb muscles, whilst leaving intact excitation transmitted via a C3‐C4 propriospinal system, the descending axons of which travel in the ventral part of the funiculus. In five of the monkeys a lesion was made to the DLF at C5 which spared the ventrolateral columns. It severely reduced the monosynaptic EPSPs and disynaptic IPSPs evoked from the pyramidal tract that were present in the intact monkey spinal cord, and which might have masked the presence of disynaptic EPSPs. However, even after the lesion the proportion of motoneurones with such late EPSPs was still low (18 %); 14 % of motoneurones had EPSPs within the disynaptic range. 4 In addition, some EPSPs with relatively long segmental latencies (> 1·1 ms) were recorded before and after the C5 lesions, but since these effects could be evoked by single stimuli, had stable latencies and did not facilitate with repetitive shocks, it is likely that they represent monosynaptic EPSPs evoked by slowly conducting corticospinal fibres which survived the lesions. 5 In seven of the monkeys motoneurone responses to stimulation of the ipsilateral lateral reticular nucleus (LRN) were also tested. Most motoneurones showed EPSPs with short latencies (1·2‐2·5 ms) and other properties characteristic of monosynaptic activation. This is consistent with the presence of collaterals of C3‐C4 propriospinal neurones to the LRN, as demonstrated in the cat. 6 These short‐latency EPSPs evoked from the LRN were just as common before (77 %) as after (75 %) the C5 lesion. They had small amplitudes both before (mean ± s.d. 1·1 ± 0·59 mV) and after (1·2 ± 0·72 mV) the lesion. Unlike the situation in the cat, only a small proportion (16 %) of motoneurones activated from the LRN showed late EPSPs after repetitive stimulation of the pyramid. 7 The results provide little evidence for significant corticospinal excitation of motoneurones via a system of C3‐C4 propriospinal neurones in the monkey. The general absence of responses mediated by such a system in the macaque, under experimental conditions similar to those in which they are seen in the cat, show that extrapolation of results from the cat to the primate should be made with considerable caution.

Selectivity for grasp in local field potential and single neuron activity recorded simultaneously from M1 and F5 in the awake macaque monkey

The selectivity for object-specific grasp in local field potentials (LFPs) was investigated in two awake macaque monkeys trained to observe, reach out, grasp and hold one of six objects presented in a pseudorandom order. Simultaneous, multiple electrode recordings were made from the hand representations of primary motor cortex (M1) and ventral premotor cortex (area F5). LFP activity was well developed during the observation and hold periods of the task, especially in the beta-frequency range (15–30 Hz). Selectivity of LFP activity for upcoming grasp was rare in the observation period, but common during stable grasp. The majority of M1 (90 of 92) and F5 (81of 97) sites showed selectivity for at least one frequency, which was maximal in the beta range but also present at higher frequencies (30–50 Hz). When the LFP power associated with grasp of a specific object was large in the beta-frequency range, it was usually of low power in the higher 30–50 Hz range, and vice-versa. Simple hook grips involving flexion of one or more fingers were associated with large beta power, whereas more complex grips involving the thumb (e.g., precision grip) were associated with small beta power. At many M1 sites, there was a highly significant inverse relationship between the tuning of spikes (including those of identified pyramidal tract neurons) and beta-range LFP for different grasps, whereas a positive correlation was found at higher frequencies (30–50 Hz). High levels of beta LFP and low pyramidal cell spike rate may reflect a common mechanism used to control motor set during different types of grasp.

Task-dependent modulations of cortical oscillatory activity in human subjects during a bimanual precision grip task

Oscillations are a widespread feature of normal brain activity and have been reported at a variety of different frequencies in different neuronal systems. The demonstration that oscillatory activity is present in motor command signals has prompted renewed interest in the possible functions of synchronous oscillatory activity within the primate sensorimotor system. In the current study, we investigated task-dependent modulations in coupling between sensorimotor cortical oscillators during a bimanual precision grip task. The task required a hold-ramp-hold pattern of grip force to be exerted on a compliant object with the dominant right hand, while maintaining a steady grip with the nondominant hand. We found significant task-related modulation of 15- to 30-Hz coherence between magnetoencephalographic (MEG) activity recorded from the left sensorimotor cortex and electromyographic (EMG) activity in hand muscles on the right side. This coherence was maximal during steady hold, but disappeared during the ramp movements. Interestingly coherence between the right sensorimotor MEG and left-hand EMG showed a similar, although less deeply modulated, task-related pattern, even though this hand was maintaining a simple steady grip. No significant ipsilateral MEG-EMG coherence was observed in the 15- to 30-Hz passband for either hand. These results suggest that the cortical oscillators in the two sensorimotor cortices are independent to some degree but that they may share a common mechanism that attenuates the cortical power in both hemispheres in the 15- to 30-Hz range during movements of one hand. The results are consistent with the hypothesis that oscillatory activity in the motor system is important in resetting the descending motor commands needed for changes in motor state, such as those that occur in the transition from movement to steady grip.

TASK-RELATED VARIATION IN CORTICOSPINAL OUTPUT EVOKED BY TRANSCRANIAL MAGNETIC STIMULATION IN THE MACAQUE MONKEY

1. A volley evoked by transcranial magnetic stimulation (TMS) over the motor cortex was recorded from the medullary pyramid in an awake monkey performing a precision grip task. It was identified as corticospinal using a collision test. 2. The volley latency was 0.50 ms, indicating that it was produced by direct activation of corticospinal neurones. 3. A mean modulation of 13% in the amplitude of this volley was seen during task performance, with the largest volley occurring during the hold phase of the task. A similar pattern of modulation was seen in the EMG responses of hand and forearm muscles to TMS. 4. No comparable modulation was observed in a volley evoked by electrical stimulation of the corticospinal fibres via chronically implanted electrodes in the cerebral peduncle. 5. The results are compatible with direct activation of the corticospinal neurones by TMS at a site close to the soma, with the probability of activation by TMS depending on the current level of cortical excitability.

A novel algorithm to remove electrical cross‐talk between surface EMG recordings and its application to the measurement of short‐term synchronisation in humans

Pairs of discharges of single motor units recorded in the same or different muscles often show synchronisation above chance levels. If large numbers of units are synchronous within and between muscles then the synchrony will be measurable in population recordings such as surface EMG. Measuring synchrony between surface EMG recordings has a number of practical and scientific advantages compared with single motor units recorded from intramuscular electrodes. However, the measurement of such synchrony in the time domain between surface EMGs is complicated because the recordings are contaminated by electrical cross‐talk. In this study we recorded surface EMG simultaneously from five hand and forearm muscles during a precision grip task. Using a novel ‘blind signal separation’ algorithm, we were able to remove electrical cross‐talk. The cross‐talk‐corrected EMGs could then be used to assess task‐dependent modulation in both oscillatory (15‐30 Hz) and non‐oscillatory synchrony (all other frequencies). In agreement with previous studies, the oscillatory component was maximal during steady holding but abolished during movement. By contrast, the non‐oscillatory component of the EMG synchrony appeared remarkably constant throughout all phases of the task. We conclude that surface EMG recordings can be of considerable use in the assessment of population synchrony changes, providing that electrical cross‐talk between nearby channels is removed using a statistical signal processing technique. Our results show a striking difference in the task‐dependent modulation of oscillatory and non‐oscillatory synchrony between muscles during a dynamic precision grip task.

An investigation of the intrinsic circuitry of the motor cortex of the monkey using intra-cortical microstimulation.

Abstract The motor cortex contains a distributed map of muscles, with a single muscle represented over a wide cortical area. We have searched for inter-connections between distant sites projecting to common muscles by delivering pairs of 20-µA single-pulse intracortical microstimuli (ICMS) to sites separated by 1.5–2 mm in the hand-area primary motor cortex of two macaque monkeys performing a precision grip task. The facilitation of hand- and forearm-muscle rectified EMG was measured. When stimuli were delivered simultaneously, responses were quantified using a technique to correct for non-linearities inherent in the use of averaged, rectified EMG. A spatial facilitation was seen for such simultaneous stimuli; however, it was of the same magnitude as that occurring when ICMS was paired with stimulation of corticospinal axons in the pyramidal tract (PT), so that it was likely to be spinal in origin. When two such distant sites were stimulated separated by a 10- or 20-ms delay, the second response scaled with the level of background EMG in the same way as a response to the PT stimulus. By contrast, when the same site was stimulated twice with these delays, the second response showed a facilitation compared with a similarly timed PT response. There would therefore appear to be a local facilitation of the cortical output at these intervals, which is not seen between distant sites. Antidromically identified pyramidal-tract neurones (PTNs) were recorded whilst stimuli were delivered to a cortical site, with a distance between stimulating and recording electrodes of also 1.5–2 mm. The most common response was a facilitation followed by a suppression. Six of eleven PTNs showed a facilitation in their discharge following this stimulation (maximum connection strength s=0.19), 8/11 showed a suppression (maximum s=0.16). It is concluded that powerful inter-connections do exist between distributed parts of the motor output and that there is widespread cortical activation after even a single ICMS pulse. However, these inter-connections do not lead to interactions between cortical outputs following stimulation, as assessed from the EMG. It is proposed that this is likely to reflect differences in the summation of output cells to local versus remote stimulation.

The structure and function of the developing corticospinal tract : somme key issues.

Publisher Summary This chapter explains some of the key issues regarding the structure and function of the developing corticospinal tract. Abnormal development of descending motor systems is associated with a variety of movement disorders. In primates, some corticospinal neurones establish a monosynaptic linkage between the primary motor cortex and spinal motoneurones, particularly those innervating hand and finger muscles. The use of electrophysiological approaches to prove the existence of a monosynaptic connection that requires intracellular recording from the target motoneurones. The monosynaptic origin of the excitatory postsynaptic potential (EPSP) is indicated when the segmental delay between the arrival of the tract volley and EPSP onset is too short to involve more than one synapse. The chapter also examines the change in axon diameter of the corticospinal neurons change during development and its relation to conduction velocity. The myelination of corticospinal axons is a postnatal process clearly protracted with respect to that of the other descending pathways. This period of myelination far outlasts that in which the spinal gray matter receives corticospinal innervation. In primates, corticospinal axons seem to be myelinated over their cranial before their spinal course. In the spinal cord, myelination of the corticospinal tract follows a rostral-to-caudal gradient. The chapter also elaborates the use of transcranial magnetic stimulation for studying corticospinal development.