Persistent sparing of action conceptual processing in spite of increasing disorders of action production: A case against motor embodiment of action concepts

ABSTRACT

In this study, we addressed the issue of whether the brain sensorimotor circuitry that controls action production is causally involved in representing and processing action-related concepts. We examined the three-year pattern of evolution of brain atrophy, action production disorders, and action-related concept processing in a patient (J.R.) diagnosed with corticobasal degeneration. During the period of investigation, J.R. presented with increasing action production disorders resulting from increasing bilateral atrophy in cortical and subcortical regions involved in the sensorimotor control of actions (notably, the superior parietal cortex, the primary motor and premotor cortex, the inferior frontal gyrus, and the basal ganglia). In contrast, the patient's performance in processing action-related concepts remained intact during the same period. This finding indicated that action concept processing hinges on cognitive and neural resources that are mostly distinct from those underlying the sensorimotor control of actions.     

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.     

Association study between two novel single nucleotide polymorphisms and sporadic Parkinson's disease in Chinese Han population

Mirror neurons are thought to facilitate emotion processing, but it is unclear whether the valence of an emotional presentation (positive or negative) can influence subsequent mirror neuron activity. Participants completed a transcranial magnetic stimulation experiment that involved stimulation of the primary motor cortex, and electromyography recording from contralateral hand muscles. This was performed while participants viewed videos of either a static hand or a transitive hand action preceded by either a positive or negative stimulus. Corticospinal excitability facilitation during action observation was significantly greater following the presentation of negative (relative to positive) stimuli; this was evident for the first dorsal interosseous muscle (which was central to the observed grasp), but not for the abductor digiti minimi muscle. This study provides evidence that emotional valence can modulate mirror neuron activity, which may reflect an adaptive mechanism.     

Brain activity related to serial cognitive performance resembles circuitry of higher order motor control

Differences between two states of cerebral activation were studied in eight subjects by positron emission tomography (PET) of regional cerebral blood flow (rCBF) and subsequent statistical parameter mapping. Subjects had to respond to a row of numbers presented on tape. In one condition they had to repeat each number. In the other condition the last heard number had to be added to the number presented before. Cerebral activity specifically related to the serial addition task was distributed over supplementary motor area (SMA), left premotor cortex and superior dorsal parietal cortex bilaterally, without significant involvement of prefrontal cortex. This indicated circuitry related to mental performance characterised by a fixed strategy of executing serial manipulation of numbers within internal space. The main aim of this communication is to discuss the similarity between circuitry underlying higher order motor control and pure cognitive performance.     

Passive reading and motor imagery about hand actions and tool-use actions: an fMRI study

Recent studies have shown that motor activations in action verb comprehension can be modulated by task demands (e.g., motor imagery vs. passive reading) and the specificity of action verb meaning. However, how the two factors work together to influence the involvement of the motor system during action verb comprehension is still unclear. To address the issue, the current study investigated the brain activations in motor imagery and passive reading of verbs about hand actions and tool-use actions. Three types of Chinese verbs were used, including hand-action verbs and two types of tool-use verbs emphasizing either the hand or tools information. Results indicated that all three types of verbs elicited common activations in hand motor areas during passive reading and motor imagery. Contrast analyses showed that in the hand verbs and the tool verbs where the hand information was emphasized, motor imagery elicited stronger effects than passive reading in the superior frontal gyrus, supplemental motor area and cingulate cortex that are related to motor control and regulation. For tool-use verbs emphasizing tools information, the motor imagery task elicited stronger activity than passive reading in occipital regions related to visual imagery. These results suggest that motor activations during action verb comprehension can be modulated by task demands and semantic features of action verbs. The sensorimotor simulation during language comprehension is flexible and determined by the interactions between linguistic and extralinguistic contexts.     

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).     

Sensory-motor interference abolishes repetition priming for observed actions,but not for action-related verbs

Several studies on humans have shown a recruitment of the sensory-motor system in the perception of action-related visual and verbal material, suggesting that actions are represented through sensory-motor processes. To date, these studies have not disentangled whether such a recruitment is epiphenomenal or necessary to action representation. Here we took advantage of repetition priming as a tool to investigate the cognitive representation of actions, and systematically looked whether a concurrent motor or verbal task had a detrimental effect on this representation. In a first experiment participants discriminated images depicting meaningless and meaningful actions, while performing either a concurrent sensory-motor or an articulatory suppression task. Images were classified as depicting a repeated or a new action, relative to the previous image in the trial series. We found a facilitation by repetition priming, that was unaffected by the articulatory task but was completely abolished by the sensory-motor task. In a second experiment, we investigated whether the sensory-motor system is also causally involved in processing action-related verbs. In this experiment actions were presented as written infinitive verbs rather than as images. The facilitation by repetition priming was again unaffected by the concurrent articulatory task, while the sensory-motor concurrent task, although reducing the facilitation, did not abolish it. Our data provide evidence that the sensory-motor system is differentially involved during visual processing of actions and during processing of action-related verbs. Results are discussed within the theoretical frame of embodied cognition.     

Attention to movement modulates activity in sensori-motor areas,including primary motor cortex

Attention to sensory stimulation modulates behavioural responses and cortical activity. Attention to movement can also modulate motor responses. For example, directing attention away from cued movements can increase reaction times. This study used fMRI to determine where in the motor cortex attention to movement modulates activity. Attention to movement was reduced by asking subjects to perform a concurrent distractor task (counting backwards). Sensori-motor areas showing a negative interaction between counting and movement (i.e. reduced activation in the dual task condition relative to the sum of the single task conditions) included the supplementary motor area (SMA), cingulate cortex, insula and post-central gyrus. A separate volumes-of-interest analysis revealed significant reductions in mean percent signal change in the dual task compared to the single task in a portion of the pre-central gyrus, deep in the central sulcus (thought to correspond to area 4p) and SMA. We conclude that the brain network for motor control is modulated by attention at multiple sites, including the primary motor cortex. These results are also discussed with reference to theories concerning the neural correlates of dual task performance and mental calculation and have implications for the interpretation of functional imaging studies of normal and impaired motor performance.     

Control of action as mediated by the human frontal lobe

Conscious control of action involves the voluntary initiation and the continuous adjustment of motor activity. Neuroimaging data provide evidence that the plan for a movement is developed with respect to the behavioral context in prefrontal cortex, while the synergies of a motor program are coded by premotor cortex and the specific movement parameters by the motor cortex. It is suggested that the initiational aspects of conscious motor activity are implemented in a medial system of information flow and the integrative aspects in a lateral system of the human frontal lobe.     

Effects of hand movement path on motor cortical activity in awake,behaving rhesus monkeys

Summary Neuronal activity was studied in the primary (M1), supplementary (M2), dorsal premotor (PMd), and ventral premotor (PMv) cortex of awake, behaving rhesus monkeys. The animals performed forelimb movements to three targets, each approached by three different types of trajectories. With one trajectory type, the monkey moved its hand straight to the target, with another, the path curved in a clockwise direction, and with a third, the path curved in a counter-clockwise direction. We examined whether neuronal activity in these areas exclusively reflects a hand movement's net distance and direction or, alternatively, whether other factors also influence cortical activity. It was found that neuronal activity during all phases of a trial reflects aspects of movement in addition to target location. Among these aspects may be selection of an integrated motor act from memory, perhaps specifying the entirety of a path by which the hand moves to a target.     

猴大脑内侧皮质运动区投射到运动前区的神经元的分布

目的定性和定量解析内侧皮质运动区投射到运动前区不同部位神经元的分布。方法采用多重标记法在同一只猴运动前区(PM)的三个不同部位即吻背侧部(PMdr)、尾背侧部(PMdc)及腹侧部(PMv)分别注入DY、FB、WGA-HRP三种不同的逆行标记物,对在内侧皮质运动区(MMC)逆行标记神经元的分布进行精确的定位和定量分析。结果投射到PMdr的神经元主要分布在前辅助运动区(prp-SMA)及前扣带回皮质运动区(CMAr);投射到PMdc的神经元,在MMC均有不同的分布,但在后扣带回皮质运动区(CMAc)被标记的神经元量明显多于其它部位;投射到PMv的神经元主要分布在辅助运动区(SMA)和CMAc,在CMAr也有少量标记神经元。结论SMA和CMAc主要投射到PMv,PMdr多接受pre-SMA和CMAr的投射。     

Transcranial magnetic stimulation of the primary motor cortex modulates response interference in a flanker task

In a typical flanker task, responses to a central target (“S” or “N”) are modulated by whether the flankers are compatible (“SSSSS”) or incompatible (“NNSNN”), with increased reaction times and decreased accuracy on incompatible trials. The role of the motor system in response interference under these conditions remains unclear, however. Here we show that transcranial magnetic stimulation (TMS) of the left primary motor cortex modulates the amount of flanker interference depending on the hand used for the response. Left motor TMS delivered at 200 ms after the onset of the array increased interference from incompatible flankers (“SSNSS”) when the target response was associated with the contralateral motor response (i.e. for “N” responses with the right hand), relative to when responses were to targets using the (left) hand ipsilateral to the site of TMS. Interestingly, under identical conditions, the degree of flanker interference was reduced when the TMS pulse was applied later in time. The analyses of the TMS-induced motor evoked potentials pointed to motor activity varying in the same conditions. We discuss the implications for understanding response interference and the role of the primary motor cortex in response selection.     

Branching thalamic afferents link action and perception

Recent observations of single axons and review of older literature show that axons afferent to the thalamus commonly branch, sending one branch to the thalamus and another to a motor or premotor center of the brain stem. That is, the messages that the thalamus relays to the cerebral cortex can be regarded as copies of motor instructions. This pattern of axonal branching is reviewed, particularly for the somatosensory and the visual pathways. The extent to which this anatomical evidence relates to views that link action to perception is explored. Most pathways going through the thalamus to the cortex are already involved in motor mechanisms. These motor links occur before and during activity in the parallel and hierarchical corticocortical circuitry that currently forms the focus of many studies of perceptual processing.     

Visually cued motor synchronization: modulation of fMRI activation patterns by baseline condition

A well-known issue in functional neuroimaging studies, regarding motor synchronization, is to design suitable control tasks able to discriminate between the brain structures involved in primary time-keeper functions and those related to other processes such as attentional effort. The aim of this work was to investigate how the predictability of stimulus onsets in the baseline condition modulates the activity in brain structures related to processes involved in time-keeper functions during the performance of a visually cued motor synchronization task (VM). The rational behind this choice derives from the notion that using different stimulus predictability can vary the subject's attention and the consequently neural activity. For this purpose, baseline levels of BOLD activity were obtained from 12 subjects during a conventional-baseline condition: maintained fixation of the visual rhythmic stimuli presented in the VM task, and a random-baseline condition: maintained fixation of visual stimuli occurring randomly. fMRI analysis demonstrated that while brain areas with a documented role in basic time processing are detected independent of the baseline condition (right cerebellum, bilateral putamen, left thalamus, left superior temporal gyrus, left sensorimotor cortex, left dorsal premotor cortex and supplementary motor area), the ventral premotor cortex, caudate nucleus, insula and inferior frontal gyrus exhibited a baseline-dependent activation. We conclude that maintained fixation of unpredictable visual stimuli can be employed in order to reduce or eliminate neural activity related to attentional components present in the synchronization task.     

Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys

The goal of the present neuroanatomical study in macaque monkeys was twofold: (1) to clarify whether the hand representation of the primary motor cortex (M1) has a transcallosal projection to M1 of the opposite hemisphere; (2) to compare the topography and density of transcallosal connections for the hand representations of M1 and the supplementary motor area (SMA). The hand areas of M1 and the SMA were identified by intracortical microstimulation and then injected either with retrograde tracer substances in order to label the neurons of origin in the contralateral motor cortical areas (four monkeys) or, with an anterograde tracer, to establish the regional distribution and density of terminal fields in the opposite motor cortical areas (two monkeys). The main results were: (1) The hand representation of M1 exhibited a modest homotopic callosal projection, as judged by the small number of labeled neurons within the region corresponding to the contralateral injection. A modest heterotopic callosal projection originated from the opposite supplementary, premotor, and cingulate motor areas. (2) In contrast, the SMA hand representation showed a dense callosal projection to the opposite SMA. The SMA was found to receive also dense heterotopic callosal projections from the contralateral rostral and caudal cingulate motor areas, moderate projections from the lateral premotor cortex, and sparse projections from M1. (3) After injection of an anterograde tracer (biotinylated dextran amine) in the hand representation of M1, only a few small patches of axonal label were found in the corresponding region of M1, as well as in the lateral premotor cortex; virtually no label was found in the SMA or in cingulate motor areas. Injections of the same anterograde tracer in the hand representation of the SMA, however, resulted in dense and widely distributed axonal terminal fields in the opposite SMA, premotor cortex, and cingulate motor areas, while labeled terminals were clearly less dense in M1. It is concluded that the hand representations of the SMA and M1 strongly differ with respect to the strength and distribution of callosal connectivity with the former having more powerful and widespread callosal connections with a number of motor fields of the opposite cortex than the latter. These anatomical results support the proposition of the SMA being a bilaterally organized system, possibly contributing to bimanual coordination.On leave from the Institute of Physiology, Armenian Academy of Sciences, Erevan, Armenia     

Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex

The cerebellum, parietal cortex, and premotor cortex are integral to visuomotor processing. The parameters of visual information that modulate their role in visuomotor control are less clear. From motor psychophysics, the relation between the frequency of visual feedback and force variability has been identified as nonlinear. Thus we hypothesized that visual feedback frequency will differentially modulate the neural activation in the cerebellum, parietal cortex, and premotor cortex related to visuomotor processing. We used functional magnetic resonance imaging at 3 Tesla to examine visually guided grip force control under frequent and infrequent visual feedback conditions. Control conditions with intermittent visual feedback alone and a control force condition without visual feedback were examined. As expected, force variability was reduced in the frequent compared with the infrequent condition. Three novel findings were identified. First, infrequent (0.4 Hz) visual feedback did not result in visuomotor activation in lateral cerebellum (lobule VI/Crus I), whereas frequent (25 Hz) intermittent visual feedback did. This is in contrast to the anterior intermediate cerebellum (lobule V/VI), which was consistently active across all force conditions compared with rest. Second, confirming previous observations, the parietal and premotor cortices were active during grip force with frequent visual feedback. The novel finding was that the parietal and premotor cortex were also active during grip force with infrequent visual feedback. Third, right inferior parietal lobule, dorsal premotor cortex, and ventral premotor cortex had greater activation in the frequent compared with the infrequent grip force condition. These findings demonstrate that the frequency of visual information reduces motor error and differentially modulates the neural activation related to visuomotor processing in the cerebellum, parietal cortex, and premotor cortex.     

Low frequency rTMS effects on sensorimotor synchronization

Previous studies using low frequency (1 Hz) rTMS over the motor and premotor cortex have examined repetitive movements, but focused either on motor aspects of performance such as movement speed, or on variability of the produced intervals. A novel question is whether TMS affects the synchronization of repetitive movements with an external cue (sensorimotor synchronization). In the present study participants synchronized finger taps with the tones of an auditory metronome. The aim of the study was to examine whether motor and premotor cortical inhibition induced by rTMS affects timing aspects of synchronization performance such as the coupling between the tap and the tone and error correction after a metronome perturbation. Metronome sequences included perturbations corresponding to a change in the duration of a single interval (phase shifts) that were either small and below the threshold for conscious perception (10 ms) or large and perceivable (50 ms). Both premotor and motor cortex stimulation induced inhibition, as reflected in a lengthening of the silent period. Neither motor nor premotor cortex rTMS altered error correction after a phase shift. However, motor cortex stimulation made participants tap closer to the tone, yielding a decrease in tap-tone asynchrony. This provides the first neurophysiological demonstration of a dissociation between error correction and tap-tone asynchrony in sensorimotor synchronization. We discuss the results in terms of current theories of timing and error correction.     

Action-Related Speech Modulates Beta Oscillations During Observation of Tool-Use Gestures

Language and action have been thought of as closely related. Comprehending words or phrases that are related to actions commonly activates motor and premotor areas, and this comprehension process interacts with action preparation and/or execution. However, it remains unclear whether comprehending action-related language interacts with action observation. In the current study, we examined whether the observation of tool-use gesture subjects to interaction with language. In an electroencephalography (EEG) study (n?=?20), participants were presented with video clips of an actor performing tool-use (TU, e.g., hammering with a fist) and emblematic (EM, e.g., the thumb up sign for ‘good job’) gestures accompanied by either comprehensible German (G) or incomprehensible Russian sentences (R). Participants performed a semantic judging task, evaluating whether the co-speech gestures were object- or socially-related. Behavioral results from the semantic task showed faster response for the TU versus EM gestures only in the German condition. For EEG, we found that TU elicited beta power decrease (~?20 Hz) when compared to EM gestures, however this effect was reduced when gestures were accompanied by German instead of Russian sentences. We concluded that the processing of action-related sentences might facilitate gesture observation, in the sense that motor simulation required for TU gestures, as indexed by reduced beta power, was modulated when accompanied by comprehensible German speech. Our results corroborate the functional role of the beta oscillations during perception of hand gestures, and provide novel evidence concerning language–motor interaction.     

Hand-related action words impair action anticipation in expert table tennis players: Behavioral and neural evidence

Athletes extract kinematic information to anticipate action outcomes. Here, we examined the influence of linguistic information (experiment 1, 2) and its underlying neural correlates (experiment 2) on anticipatory judgment. Table tennis experts and novices remembered a hand- or leg-related verb or a spatial location while predicting the trajectory of a ball in a video occluded at the moment of the serve. Experiment 1 showed that predictions by experts were more accurate than novices, but experts’ accuracy significantly decreased when hand-related words versus spatial locations were memorized. For nonoccluded videos with ball trajectories congruent or incongruent with server actions in experiment 2, remembering hand-related verbs shared cognitive resources with action anticipation only in experts, with heightened processing load (increased P3 amplitude) and more efficient conflict monitoring (decreased N2 amplitude) versus leg-related verbs. Thus, action anticipation required updating of motor representations facilitated by motor expertize but was also affected by effector-specific semantic representations of actions, suggesting a link from language to motor systems.