Neural activation in cognitive motor processes: comparing motor imagery and observation of gymnastic movements

The simulation concept suggested by Jeannerod (Neuroimage 14:S103-S109, 2001) defines the S-states of action observation and mental simulation of action as action-related mental states lacking overt execution. Within this framework, similarities and neural overlap between S-states and overt execution are interpreted as providing the common basis for the motor representations implemented within the motor system. The present brain imaging study compared activation overlap and differential activation during mental simulation (motor imagery) with that while observing gymnastic movements. The fMRI conjunction analysis revealed overlapping activation for both S-states in primary motor cortex, premotor cortex, and the supplementary motor area as well as in the intraparietal sulcus, cerebellar hemispheres, and parts of the basal ganglia. A direct contrast between the motor imagery and observation conditions revealed stronger activation for imagery in the posterior insula and the anterior cingulate gyrus. The hippocampus, the superior parietal lobe, and the cerebellar areas were differentially activated in the observation condition. In general, these data corroborate the concept of action-related S-states because of the high overlap in core motor as well as in motor-related areas. We argue that differential activity between S-states relates to task-specific and modal information processing.     

The embodied nature of motor imagery: the influence of posture and perspective

It is assumed that imagining oneself from a first-person perspective (1PP) is more embodied than a third-person perspective (3PP). Therefore, 1PP imagery should lead to more activity in motor and motor-related structures, and the postural configuration of one’s own body should be particularly relevant in 1PP simulation. The present study investigated whether proprioceptive information on hand position is integrated similarly in 1PP and 3PP imagery of hand movements. During functional magnetic resonance imaging (fMRI) scanning, 20 right-handed female college students watched video sequences of different hand movements with their right hand in a compatible versus incompatible posture and subsequently performed 1PP or 3PP imagery of the movement. Results showed stronger activation in left hemisphere motor and motor-related structures, especially the inferior parietal lobe, on 1PP compared with 3PP trials. Activation in the left inferior parietal lobe (parietal operculum, SII) and the insula was stronger in 1PP trials with compatible compared with incompatible posture. Thus, proprioceptive information on actual body posture is more relevant for 1PP imagery processes. Results support the embodied nature of 1PP imagery and indicate possible applications in athletic training or rehabilitation.     

The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions

We investigated the properties of the neural response to transcranial magnetic stimulation (TMS) applied over the human primary motor cortex. Consistent with our previous findings, single pulses of TMS induce a characteristic negative deflection at 45 ms (N45) and a transient oscillation in the beta frequency-range (15–30 Hz), as measured using electroencephalograpy (EEG). Here we show the relative specificity of the beta oscillation and the N45; both are stronger when elicited by stimulation applied over the primary motor cortex, as compared with stimulation over the dorsal premotor cortex. We also provide a quantitative analysis of the beta responses to single pulses of TMS and show that the responses are highly phaselocked to the TMS pulses within single subjects; this phaselocking is similar from subject to subject. A single pulse of TMS applied over the primary motor cortex thus appears to reset the ongoing oscillations of the neurons, bringing them transiently into synchrony. Finally, we examine the effect of local or distal modulation of the excitability of the primary motor cortex on the beta oscillation and the N45 in response to single-pulse TMS. We applied low-frequency subthreshold repetitive TMS either over the primary motor cortex (local modulation) or, on a separate day, over the dorsal premotor cortex (distal modulation). The modulation was evaluated with single suprathreshold test pulses of TMS applied over the primary motor cortex before and after the subthreshold low-frequency rTMS. We recorded the EEG response throughout the testing session, i.e. to both the subthreshold and the suprathreshold pulses. After repetitive TMS applied over the primary motor cortex, but not the dorsal premotor cortex, the amplitude of the N45 in response to suprathreshold pulses tended to decrease (not significant), and subsequently increased (significant); neither type of repetitive TMS affected the amplitude of the beta oscillation. We conclude that (1) the N45 depends on circuits intrinsic to the primary motor cortex; (2) the beta oscillation is specific to stimulation of the primary motor cortex, but is not affected by modulation of either cortical area and; (3) the beta oscillatory response to pulses of TMS arises from resetting of ongoing oscillations rather than their induction.The first author was funded by a fellowship from the Canadian Institute of Health Research (CIHR).     

Persistent motor system abnormalities in formerly concussed athletes

Context:

The known detrimental effects of sport concussions on motor system function include balance problems, slowed motor execution, and abnormal motor cortex excitability.

Objective:

To assess whether these concussion-related alterations of motor system function are still evident in collegiate football players who sustained concussions but returned to competition more than 9 months before testing.

Design:

Case-control study.

Setting:

University laboratory.

Patients or Other Participants:

A group of 21 active, university-level football players who had experienced concussions was compared with 15 university football players who had not sustained concussions.

Intervention(s):

A force platform was used to assess center-of-pressure (COP) displacement and COP oscillation regularity (approximate entropy) as measures of postural stability in the upright position. A rapid alternating-movement task was also used to assess motor execution speed. Transcranial magnetic stimulation over the motor cortex was used to measure long-interval intracortical inhibition and the cortical silent period, presumably reflecting γ-aminobutyric acid subtype B receptor-mediated intracortical inhibition.

Main Outcome Measure(s):

COP displacement and oscillation regularity, motor execution speed, long-interval intracortical inhibition, cortical silent period.

Results:

Relative to controls, previously concussed athletes showed persistently lower COP oscillation randomness, normal performance on a rapid alternating-movement task, and more M1 intracortical inhibition that was related to the number of previous concussions.

Conclusions:

Sport concussions were associated with pervasive changes in postural control and more M1 intracortical inhibition, providing neurophysiologic and behavioral evidence of lasting, subclinical changes in motor system integrity in concussed athletes.     

A voxel-by-voxel parametric fMRI study of motor mental rotation: hemispheric specialization and gender differences in neural processing efficiency

Differences between men and women in brain size, cognitive performance and lateralization of brain activation have been perennial and controversial issues. Here we show that in a motor mental rotation task where women and men performed equally well, the slope of the functional magnetic resonance imaging (fMRI) blood oxygenation level dependent (BOLD) signal per degree of mental rotation was overall 2.4× higher in men than in women. This was attributed to the much more inefficient engagement (i.e. higher slopes) of the right hemisphere by men (mainly the frontal lobe). These findings indicate that women process information much more efficiently than men, which could offset smaller brain size.     

Monoamine content in the motor cortex after injury to the opposite motor cortex

In chronic experiments on eight cats a spectrofluorometric study was made of the serotonin, dopamine, and noradrenalin content in the sigmoid cortex of the left cerebral hemisphere 2, 3, 4, and 5–8 days after removal of the symmetrical cortex of the right hemisphere. A decrease in the dopamine content and a tendency for a decrease in the noradrenalin and serotonin content were observed on the 2nd day, at the time of maximal disturbances of locomotor function. On the 3rd–4th and 5th–8th days, during the period of recovery of motor activity, the serotonin level increased, the dopamine content remained low, whereas the noradrenalin level rose considerably. The role of biochemical changes in the motor cortex in the mechanisms of recovery of locomotor function after injury to the symmetrical cortical region is discussed.Laboratory of Pathophysiology of Neurohumoral Regulation, Institute of General Pathology and Pathophysiology, Academy of Medical Sciences of the USSR, Moscow. (Presented by Academician of the Academy of Medical Sciences of the USSR A. M. Chernukh.) Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 86, No. 9, pp. 270–271, September, 1978.     

Hemispheric asymmetry in cerebrovascular reactivity of the human primary motor cortex: an in vivo study at 7 T

Current functional MRI (fMRI) approaches assess underlying neuronal activity through monitoring the related local variations in cerebral blood oxygenation, blood volume and blood flow. This vascular response is likely to vary across brain regions and across individuals, depending on the composition of the local vascular bed and on the vascular capacity to dilate. The most widely used technique uses the blood oxygen level dependent (BOLD) fMRI signal, which arises from a complex combination of all of these factors. The model of handedness provides a case where one brain region (dominant motor cortex) is known to have a stronger BOLD response over another (non‐dominant motor cortex) during hand motor task performance. We predict that this is accompanied by a higher vascular reactivity in the dominant motor cortex, when compared with the non‐dominant motor cortex. Precise measurement of end‐tidal CO₂ and a novel sinusoidal CO₂ respiratory challenge were combined with the high sensitivity and finer spatial resolution available for fMRI at 7 T to measure BOLD cerebrovascular reactivity (CVR) in eight healthy male participants. BOLD CVR was compared between the left (dominant) and right (non‐dominant) primary motor cortices of right‐handed adults. Hemispheric asymmetry in vascular reactivity was predicted and observed in the primary motor cortex (left CVR = 0.60 ± 0.15%/mm Hg; right CVR = 0.47 ± 0.08%/mm Hg; left CVR > right CVR, P = 0.04), the first reported evidence of such a vascular difference. These findings demonstrate a cerebral vascular asymmetry between the left and right primary motor cortex. The origin of this asymmetry largely arises from the contribution of large draining veins. This work has implications for future motor laterality studies that use BOLD, and it is also suggestive of a vascular plasticity in the human primary motor cortex. Copyright © 2015 John Wiley & Sons, Ltd.     

Spatial distribution of cingulate cortical cells projecting to the primary motor cortex in the rat

We examined the location and spatial distribution of cingulate cortical cells projecting to the primary motor cortex (M1) in rats, using a double retrograde-labeling technique. The orofacial, forelimb, and hindlimb areas of M1 were physiologically identified based on the findings of intracortical microstimulation and single cell recording. Two different tracers, diamidino yellow and fast blue, were injected into two sites of M1 in each rat. Retrograde-labeled cells in the cingulate cortex were plotted with an automated plotting system. Cells projecting to the orofacial and forelimb areas of M1 were distributed in the anterior cingulate cortex (area 24) but not in the posterior cingulate cortex (retrosplenial cortex; area 29), according to topographical mapping. On the other hand, few or no cells of the cingulate cortex were observed projecting to the hindlimb area of M1. These findings suggest that the cingulate cortex projecting to the M1 in the rat are involved in the regulation of motor activity that involves the orofacial and forelimb, but not hindlimb, parts of the body.     

Roles of the rostroventromedial medulla and the spinal 5-HT1A receptor in descending antinociception induced by motor cortex stimulation in the neuropathic rat

Electric stimulation of the primary motor cortex (M1) has been effective in suppressing pain-related responses in neuropathic as well as healthy control animals. We studied whether the rostroventromedial medulla (RVM) or the spinal 5-HT_1A receptor contributes to antinociception induced by stimulation of M1 in neuropathic animals. Assessments of the noxious heat-evoked limb withdrawal reflecting spinal nociception was performed in rats with spinal nerve ligation-induced peripheral neuropathy under light pentobarbital anesthesia. Spinal antinociception induced by electric stimulation of M1 was reduced following block of the RVM with intramedullary injection of muscimol, a GABA_A receptor agonist, or following intrathecal administration of WAY-100635, a 5-HT_1A receptor antagonist. The results indicate that the RVM and the descending serotonergic pathway acting on the spinal 5-HT_1A receptor contribute to spinal antinociception induced by M1 stimulation in neuropathic animals.     

Anticipatory postural adjustment before bimanual unloading reactions: The role of the motor cortex in motor learning

The role of the motor cortex in forming a learned coordination (stabilization of the forearm on unloading) was studied in humans. Subjects maintained a 1-kg weight with the right (postural) forearm, the weight being attached via an electromagnet. Unloading of the postural arm was initiated by the subjects by lifting a similar load with the left arm. In control experiments, lifting of the load did not lead to unloading of the postural arm. Changes in motor cortex excitability were studied by transcranial magnetic stimulation applied to the representation area of the right biceps muscle in the motor cortex at the beginning and end of the experiments. Repeated unloading tests showed progressive decreases in the amplitude of the movement of the unloaded forearm, which were accompanied by increases in the anticipatory inhibition of the electromyogram of the biceps muscle of the unloaded arm (learning). Muscle responses to transcranial magnetic stimulation during the learning process showed no significant changes. Analysis of normalized muscle responses to transcranial magnetic stimulation (response/baseline) showed that these increased at the end of training and reached a significantly higher level than seen at the beginning of training. These results lead to the conclusion that the motor cortex plays a fundamental role in inhibiting synergies and coordinations which would interfere with the formation of the new coordination during motor learning. __________ Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 56, No. 5, pp. 603–610, September–October, 2006.     

Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex

It is an important issue to address the mode of information processing in the somatic motor circuit linking the frontal cortex and the basal ganglia. In the present study, we investigated the extent to which corticostriatal input zones from the primary motor cortex (MI), the supplementary motor area (SMA), and the premotor cortex (PM) of the macaque monkey might overlap in the putamen. Intracortical microstimulation was performed to map the MI, SMA, and dorsal (PMd) and ventral (PMv) divisions of the PM. Then, two different anterograde tracers were injected separately into somatotopically corresponding regions of two given areas of the MI, SMA, PMd, and PMv. With respect to the PMd and PMv, tracer injections were centered on their forelimb representations. Corticostriatal input zones from hindlimb, forelimb, and orofacial representations of the MI and SMA were, in this order, arranged from dorsal to ventral within the putamen. Dense input zones from the MI were located predominantly in the lateral aspect of the putamen, whereas those from the SMA were in the medial aspect of the putamen. On the other hand, corticostriatal inputs from forelimb representations of the PMd and PMv were distributed mainly in the dorsomedial sector of the putamen. Thus, the corticostriatal input zones from the MI and SMA were considerably segregated though partly overlapped in the mediolateral central aspect of the putamen, while the corticostriatal input zone from the PM largely overlapped that from the SMA, but not from the MI. Received: 30 June 1997 / Accepted: 2 October 1997     

Cellular mechanisms of motor control in the vibrissal system

In this article we discuss the experimental advantages that the vibrissal motor system offers for analysis of motor control and the specializations of this system related to the unique characteristics of whisker movements. Whisker movements are often rhythmic, fast, and bilateral. Movements of individual whiskers have simple characteristics, whereas, movements of the entire vibrissae array are complex and sophisticated. In the last few years, powerful methods for high precision tracking of whisker movements have become available. The whisker musculature is arranged to permit forward movements of individual whiskers and consists—depending on the species—mainly or exclusively of fast contracting, fast fatigable muscle fibers. Whisker motor neurons are located in the lateral facial nucleus and their cellular properties might contribute to the rhythmicity of whisking. Numerous structures provide input to the lateral facial nucleus, the most mysterious and important one being the putative central pattern generator (CPG). Although recent studies identified candidate structures for the CPG, the precise identity and the functional organization of this structure remains uncertain. The vibrissa motor cortex (VMC) is the largest motor representation in the rodent brain, and recent work has clarified its localization, subdivisions, cytoarchitectonics, and connectivity. Single-cell stimulation experiments in VMC allow determining the cellular basis of cortical motor control with unprecedented precision. The functional significance of whisker movements remains to be determined.     

To eat or not to eat; regulation by the melanocortin system

The central melanocortin (MC) system is one of the best-characterized neuropeptidergic systems involved in the regulation of energy balance. This short review describes the role of the central MC system in feeding behavior. Pharmacological, anatomical and genetic studies show that activation of the MC system reduces meal size, whereas de-activation of the MC system increases meal size. Several brain regions, including distinct hypothalamic nuclei and the hindbrain, are involved in this process. Further dissection of MC pathways in feeding behavior is the subject of recent and probably future studies. As the MC system is involved in animal models of obesity and (possibly) anorexia, it appears that this is a target system for development of drugs for the treatment of disturbed human eating behavior.     

Suppression of the non-dominant motor cortex during bimanual symmetric finger movement: a functional magnetic resonance imaging study

Patterns of bimanual coordination in which homologous muscles are simultaneously active are more stable than those in which homologous muscles are engaged in an alternating fashion. This may be attributable to the stronger involvement of the dominant motor cortex in ipsilateral hand movements via interaction with the non-dominant motor system, known as neural crosstalk. We used functional magnetic resonance imaging to investigate the neural representation of the interhemispheric interaction during bimanual mirror movements. Thirteen right-handed subjects completed four conditions: sequential finger tapping using the right and left index and middle fingers, bimanual mirror and parallel finger tapping. Auditory cues (3 Hz) were used to keep the tapping frequency constant. Task-related activation in the right primary motor cortex was significantly less prominent during mirror than unimanual left-handed movements. This was mirror- and non-dominant side-specific; parallel movements did not cause such a reduction, and the left primary motor cortex showed no such differential activation across the unimanual right, bimanual mirror, and bimanual parallel conditions. Reducing the contralateral innervation of the left hand may increase the fraction of the force command to the left hand coming from the left primary motor cortex, enhancing the neural crosstalk.     

Further evidence for excitability changes in human primary motor cortex during ipsilateral voluntary contractions

The present study aimed to further investigate whether the intracortical neural circuits within the primary motor cortex (M1) are modulated during ipsilateral voluntary finger movements. Single- and paired-pulse (interstimulus intervals, ISIs; 3 ms and 12 ms) transcranial magnetic stimulations of the left M1 were applied to elicit motor evoked potential (MEP) in the right first dorsal interosseous (Rt-FDI) muscle during voluntary contractions (10% and 30% maximum voluntary contraction) of the left FDI (Lt-FDI) muscle. F-waves of Rt-FDI muscle were recorded under these left index-finger conditions for ensuring that the excitability changes occur at the supraspinal level. MEPs were also recorded during motor imagery of the left index-finger abduction instead of overt movement. The results showed that, in single-pulse transcranial magnetic stimulation (TMS) paradigm, MEPs in Rt-FDI muscle were markedly enhanced during voluntary contractions of Lt-FDI muscle compared with the complete resting state. In paired-pulse TMS paradigm, the short intracortical inhibition was significantly reduced in proportion to increments of the ipsilateral muscle contraction, whereas the intracortical facilitation had no change. F-wave of Rt-FDI muscle was unchanged under these conditions, while MEP in Rt-FDI muscle was also enhanced during motor imagery of the left index-finger abduction. Based on the present results, it is suggested that the intracortical inhibitory neural circuits may be modulated in the transition from rest to activity of the ipsilateral homonymous muscle. The excitability changes in M1 might be induced by overflows of voluntary drive given to the ipsilateral limb, probably via the transcallosal pathway.     

Contributions of the motor cortex and the cerebellum to a simple learned movement in the monkey

Monkeys were trained to perform isometric plantar flexions of the foot in a simple reaction time situation. In test sessions, the contralateral hindlimb area of the motor cortex was cooled by a cryode placed on the dura until somatosensory evoked potentials disappeared. Movement amplitude decreased to about 70% of initial size; reaction time which was measured on the EMG, and torque signals increased slightly; and the evoked response in the dentate nucleus of the cerebellum remained unchanged. An extensive lesion in the motor cortex by coagulation reduced the movement amplitude to 10% of its preoperational size, but again, did not change reaction time significantly. It is concluded that the motor cortex is not essential for the execution of this overtrained simple movement.     

Cortico-cortical mediation of short-latency (lemniscal) sensory input to the motor cortex in deeply pentobitone anaesthetized cats

In pentobarbitone-anaesthetized cats, responses were recorded as surface positive potentials in the motor cortex on forelimb and brachium conjunctivum stimulation. In such a preparation, the forelimb nerve responses are mediated via the spino-cervical tract and the dorsal column-lemniscal pathway. Lesions of the sensory cortex (sparing only the depth of the coronary sulcus) abolished or reduced short-latency peripheral responses, in the motor cortex, on both skin and muscle nerve stimulation to less than 10% of control, while brachium conjunctivum responses were unchanged. Lesions of the second somatosensory area alone reduced the motor cortex responses on peripheral nerve stimulation by 10–20%. When the sensory cortex were abolished before the spreading depression reached the recording point, as judged from the brachium conjunctivum response. The depth distribution of positive and negative field potentials, constituting the early componentsof a peripheral response in the motor cortex, closely resembled that of a cortico-cortical response evoked on stimulation in area 3. It differed from that of thalamo-cortical response evoked in brachium conjunctivum stimulation. These data suggest that most, if not all, sensory input through the dorsal column and spino-cervical tract to the motor cortex is mediatd via the sensory cortex.     

Neurophysiological examination of the corticospinal system and voluntary motor control in motor-incomplete human spinal cord injury

This study employed neurophysiological methods to relate the condition of the corticospinal system with the voluntary control of lower-limb muscles in persons with motor-incomplete spinal cord injury. It consisted of two phases. In a group of ten healthy subjects, single and paired transcranial magnetic stimulation (TMS) of the motor cortex was used to study the behavior of the resulting motor evoked potentials (MEP) in lower-limb muscles. Interstimulus intervals (ISIs) of 15–100 ms were examined for augmentation of test MEPs by threshold or subthreshold conditioning stimuli. The second phase of this study examined eight incomplete spinal cord injured (iSCI) subjects, American Spinal Injury Association Impairment Scale C (n =5) and D (n =3) in whom voluntary motor control was quantified using the surface EMG (sEMG) based Voluntary Response Index (VRI). The VRI is calculated to characterize relative output patterns across ten lower-limb muscles recorded during a standard protocol of elementary voluntary motor tasks. VRI components were calculated by comparing the distribution of sEMG in iSCI subjects with prototype patterns collected from 15 healthy subjects using the same rigidly administered protocol, The resulting similarity index (SI) and magnitude values provided the measure of voluntary motor control. Corticospinal system connections were characterized by the thresholds for MEPs in key muscles. Key muscles were those that function as the prime-movers, or agonists for the voluntary movements from which the VRI data were calculated. Results include healthy-subject data that showed significant increases in conditioned MEP responses with paired stimuli of 15–50 ms ISI. Stimulus pairs of 75 and 100 ms showed no increase in MEP peak amplitude over that of the single-pulse conditioning stimulus alone, usually no response. For the iSCI subjects, 42% of the agonists responded to single-pulse TMS and 25% required paired-pulse TMS to produce an MEP. American Spinal Injury Association Impairment Scale component motor scores for agonist muscles, Quadriceps, Tibialis Anterior, and Triceps Surae, were significantly lower where MEPs could not be obtained (p <0.05). VRI values were also significantly lower for motor tasks with agonists that had no resting MEP (p <0.01). Therefore, the presence of a demonstrable connection between the motor cortex and spinal motor neurons in persons with SCI was related to the quality of post-injury voluntary motor control as assessed by the VRI.     

Protracted postnatal development of corticospinal projections from the primary motor cortex to hand motoneurones in the macaque monkey

We have studied the development of corticospinal projections from the hand area of the primary motor cortex to the spinal cord using anterograde transport of WGA-HRP. In the neonate, as in the adult, corticospinal projections to the intermediate zone at the C8/T1 spinal level were clearly present. However, in contrast to the adult, there was only very faint and barely visible labelling in the dorso-lateral motor nuclei which supply the hand muscles. No aberrant projections to other motor nuclei were seen. By 2.5 months, a ring of dense labelling was present around the dorso-lateral motor nuclei, but labelling was still sparse in the central region. This labelling was more pronounced at 11 months, but was still not as heavy as in the adult. There was no labelling among the ventral motoneurones at any age. The conduction velocity (c.v.) of the fastest corticospinal fibres was determined in each of the monkeys. There was an age-related increase in c.v. within the spinal cord. At birth, the fastest axons had a c.v. of only 8 m·s^-1. At 11 months c.v. was still substantially slower (55 m·s^-1) than the adult value of 73 m·s^-1. In contrast, by 11 months, the axonal c.v. within the brain was close to the adult value, suggesting a rostro-caudal maturation of the corticospinal system. Our results demonstrate that corticospinal projections in the macaque monkey mature gradually over a period of at least 11 months, much longer than previously thought.