Common pathways in mental imagery and pain perception: an fMRI study of a subject with an amputated arm

The present paper reviews data from two previous studies in our laboratory, as well as some additional new data, on the neuronal representation of movement and pain imagery in a subject with an amputated right arm. The subject imagined painful and non-painful finger movements in the amputated stump while being in a MRI scanner, acquiring EPI-images for fMRI analysis. In Study I (Ersland et al., 1996) the Subject alternated tapping with his intact left hand fingers and imagining "tapping" with the fingers of his amputated right arm. The results showed increased neuronal activation in the right motor cortex (precentral gyrus) when tapping with the fingers of the left hand, and a corresponding activation in the left motor cortex when imagining tapping with the fingers of the amputated right arm. Finger tappings of the intact left hand fingers also resulted in a larger activated precentral area than imagery "finger tapping" of the amputated right arm fingers. In Study II (Rosen et al., 2001 in press) the same subject imagining painful and pleasurable finger movements, and still positions of the fingers of the amputated arm. The results showed larger activations over the motor cortex for movement imagining versus imagining the hand being in a still position, and larger activations over the sensory cortex when imagining painful experiences. It can therefore be concluded that not only does imagery activate the same motor areas as real finger movements, but also that adding instructions of pain together with imaging moving the fingers intensified the activation compared with adding instructions about non-painful experiences. From these studies, it is clear that areas activated during actual motor execution to a large extent also are activated during mental imagery of the same motor commands. In this respect the present studies add to studies of visual imagery that have shown a similar correspondence in activation between actual object perception and imagery of the same object.     

Motor imagery vividness and symptom severity in Parkinson's disease

Motor imagery (MI), the mental simulation of movement in the absence of overt motor output, has demonstrated potential as a technique to support rehabilitation of movement in neurological conditions such as Parkinson's disease (PD). Existing evidence suggests that MI is largely preserved in PD, but previous studies have typically examined global measures of MI and have not considered the potential impact of individual differences in symptom presentation on MI. The present study investigated the influence of severity of overall motor symptoms, bradykinesia and tremor on MI vividness scores in 44 individuals with mild to moderate idiopathic PD. Linear mixed effects modelling revealed that imagery modality and the severity of left side bradykinesia significantly influenced MI vividness ratings. Consistent with previous findings, participants rated visual motor imagery (VMI) to be more vivid than kinesthetic motor imagery (KMI). Greater severity of left side bradykinesia (but not right side bradykinesia) predicted increased vividness of KMI, while tremor severity and overall motor symptom severity did not predict vividness of MI. The specificity of the effect of bradykinesia to the left side may reflect greater premorbid vividness for the dominant (right) side or increased attention to more effortful movements on the left side of the body resulting in more vivid motor imagery.     

Thinking ahead: the case for motor imagery in prospective judgements of prehension

How similar are judgements concerning how we expect to perform an action, to how we actually behave? The veracity of such prospective action judgements, and the mechanisms by which they are computed, was explored in a series of tasks that involved either grasping (MC conditions) or thinking about grasping (PJ conditions) a dowel presented in various orientations. PJs concerning limits of comfortable hand supination and pronation when turning a dowel in the picture plane were highly consistent with values obtained during actual hand rotation (Exp. 1). The same was true for judgements regarding the level of awkwardness involved in adopting a prescribed grip (e.g. overhand with right hand) for dowels in various picture plane orientations (Exp. 2). When allowed to select the most natural grip (overhand versus underhand) or hand (left versus right) for engaging dowels in these orientations, subjects preferred virtually identical responses in both PJ and MC conditions. In both instances, they consistently chose the least awkward response options. As would be expected for actual movements, PJs involving awkward hand postures had longer response times (RTs), and were less accurate. Likewise, latencies for both grip and hand judgements tended to increase as a function of the angular distance between the current positions of subjects' hands, and the orientation of the chosen posture. Together, these findings are consistent with a the hypothesis that PJs involve mentally simulated actions, or motor imagery. These results suggest that motor imagery does not depend on the existence of a completed premotor plan (Jeannerod, 1994), but may instead be involved in the planning process itself. A provisional model for the involvement of imagery in motor planning is outlined, as are a set of criteria for evaluating claims of the involvement of motor imagery in problem solving.     

Cognitive constraints on motor imagery

Executed bimanual movements are prepared slower when moving to symbolically different than when moving to symbolically same targets and when targets are mapped to target locations in a left/right fashion than when they are mapped in an inner/outer fashion [Weigelt et al. (Psychol Res 71:238–447, 2007)]. We investigated whether these cognitive bimanual coordination constraints are observable in motor imagery. Participants performed fast bimanual reaching movements from start to target buttons. Symbolic target similarity and mapping were manipulated. Participants performed four action conditions: one execution and three imagination conditions. In the latter they indicated starting, ending, or starting and ending of the movement. We measured movement preparation (RT), movement execution (MT) and the combined duration of movement preparation and execution (RTMT). In all action conditions RTs and MTs were longer in movements towards different targets than in movements towards same targets. Further, RTMTs were longer when targets were mapped to target locations in a left/right fashion than when they were mapped in an inner/outer fashion, again in all action conditions. RTMTs in imagination and execution were similar, apart from the imagination condition in which participants indicated the start and the end of the movement. Here MTs, but not RTs, were longer than in the execution condition. In conclusion, cognitive coordination constraints are present in the motor imagery of fast (<1600 ms) bimanual movements. Further, alternations between inhibition and execution may prolong the duration of motor imagery.     

Deficits of anticipatory grip force control after damage to peripheral and central sensorimotor systems

Healthy subjects adjust their grip force economically to the weight of a hand-held object. In addition, inertial loads, which arise from arm movements with the grasped object, are anticipated by parallel grip force modulations. Internal forward models have been proposed to predict the consequences of voluntary movements. Anesthesia of the fingers impairs grip force economy but the feedforward character of the grip force/load coupling is preserved. To further analyze the role of sensory input for internal forward models and to characterize the consequences of central nervous system damage for anticipatory grip force control, we measured grip force behavior in neurological patients. We tested a group of stroke patients with varying degrees of impaired fine motor control and sensory loss, a single patient with complete and permanent differentation from all tactile and proprioceptive input, and a group of patients with amyotrophic lateral sclerosis (ALS) that exclusively impairs the motor system without affecting sensory modalities. Increased grip forces were a common finding in all patients. Sensory deficits were a strong but not the only predictor of impaired grip force economy. The feedforward mode of grip force control was typically preserved in the stroke patients despite their central sensory deficits, but was severely disturbed in the patient with peripheral sensory deafferentation and in a minority of stroke patients. Moderate deficits of feedforward control were also obvious in ALS patients. Thus, the function of the internal forward model and the precision of grip force production may depend on a complex anatomical and functional network of sensory and motor structures and their interaction in time and space.     

An fMRI study of temporal sequencing of motor regulation guided by an auditory cue—a comparison with visual guidance

The neuronal system to process and transfer auditory information to the higher motor areas was investigated using fMRI. Two different types of internal modulation of auditory pacing (1 Hz) were combined to design a 2×2 condition experiment, and the activation was compared with that under a visual guidance. The bilateral anterior portion of the BA22 (ant-BA22) and the left BA41/42 were more extensively activated by the combined modulation condition under the auditory cue than that under the visual cue. Among the four auditory conditions with or without the two types of internal modulation, the activation in the ant-BA22 was augmented only on the left side by the combined modulation condition. The left ant-BA22 may be especially involved in integrating the external auditory cue with internal modulation, while the activation on the right side did not depend on the complexity. The role of the left BA41/42 in motor regulation may be more specific to the processing of an auditory cue than that on the right side. These two areas in the left temporal lobe may be organized as a subsystem to handle the timing of complex movements under auditory cues, while the higher motor areas in the frontal lobe support both sensory modalities for the cue. This architecture may be considered as ‘audio-motor control’, which is similar to the visuo-motor control of the front-parietal network.     

Apraxia in a patient with atypical cerebral dominance

Liepmann postulated that the left hemisphere of right-handed persons contains the "movement formulas" that control purposeful skilled movements of the limbs on both sides of the body. Accordingly, in right-handers apraxia should follow damage to the left hemisphere, whereas right hemisphere damage should not lead to apraxia. Although this is generally true, we recently examined a right-handed man who after a right hemispheric stroke became aphasic and apraxic with his nonparalyzed right hand. Our observations suggest that the right hemisphere of this right-handed man made a critical contribution to the planning and execution of skilled movements. This case provides evidence that right-handers should not be considered a homogeneous group in terms of cerebral motor dominance and that contrary to Liepmann's postulate, hemispheric dominance for the control of skilled movements does not entirely determine handedness.     

Effects of mental imagery styles on shoulder and hip rotations during preparation of pirouettes

To analyze individual behavior in spatial navigation especially for pirouette preparations (complete whole-body rotations), the authors studied horizontal shoulder-hip interactions under 2 constraints: postural (right and left supporting legs [SL]) and spatial (clockwise [CW] and counterclockwise [CCW]). They performed kinematic analysis at the start and end of the shoulder-hip horizontal rotations (run-up) with regard to imagery of motor actions. On the basis of the Vividness of Movement Imagery Questionnaire, they classified 8 female expert ballet dancers and 7 untrained female participants according to their movement imagery style (kinesthetic and visual). At the run-up's end, the shoulders initiated the turn independently of SL but differently depending on training: CW for dancers and CCW for untrained participants (their commonly used direction). Kinesthetic and mixed imagery styles prevailed in dancers, whereas simply a mixed style appeared among untrained participants. Thus, dance training enhances the imagery of kinesthetic sensation and influences the choice of spatial direction, facilitating the body-space interaction.     

Bimanual coupling effects during arm immobilization and passive movements

When humans simultaneously perform different movements with both hands, each limb movement interferes with the contralateral limb movement (bimanual coupling). Previous studies on both healthy volunteers and patients with central or peripheral nervous lesions suggested that such motor constraints are tightly linked to intentional motor programs, rather than to movement execution. Here, we aim to investigate this phenomenon, by using a circles-lines task in which, when subjects simultaneously draw lines with the right hand and circles with the left hand, both the trajectories tend to become ovals (bimanual coupling effect). In a first group, we immobilized the subjects’ left arm with a cast and asked them to try to perform the bimanual task. In a second group, we passively moved the subjects’ left arm and asked them to perform voluntary movements with their right arm only. If the bimanual coupling arises from motor intention and planning rather than spatial movements, we would expect different results in the two groups. In the Blocked group, where motor intentionality was required but movements in space were prevented by immobilization of the arm, a significant coupling effect (i.e., a significant increase of the ovalization index for the right hand lines) was found. On the contrary, in the Passive group, where movements in space were present but motor intentionality was not required, no significant coupling effect was observed. Our results confirmed, in healthy subjects, the central role of the intentional and predictive operations, already evidenced in pathological conditions, for the occurrence of bimanual coupling.     

Interference within hands: Retrieval-induced forgetting of left and right hand movements

We examined retrieval-induced forgetting of motor sequences that were categorized by the effectors (left or right hand) involved in their execution. This left–right categorization was independent from input locations or input devices. In addition, the acquired motor sequences were arbitrarily assigned to left and right. Participants learned twelve sequential joystick movements as responses to letter stimuli. Half of the sequences pertained to the left, half to the right hand. Subsequent retrieval-practice of half the items of one hand induced forgetting for the non-retrieved rest of the items of that hand in a final recall test. This finding demonstrates that the hands were used to organize the memory storage of motor sequences in a way that gave rise to later interference between commonly stored items, that is, linked to the same hand.     

Kinematics of Goal-Directed Arm Movements in Neglect: Control of Hand Velocity

Do patients with unilateral neglect exhibit direction-specific deficits in the control of movement velocity when performing goal-directed arm movements? Five patients with left-sided neglect performed unrestrained three-dimensional pointing movements to visual targets presented at body midline, the left and right hemispace. A group of healthy adults and a group of patients with right-hemispheric brain damage but no neglect served as controls. Pointing was performed under normal room light or in darkness. Time-position data of the hand were recorded with an opto-electronic camera system. We found that compared to healthy controls, movement times were longer in both patient groups due to prolonged acceleration and deceleration phases. Tangential peak hand velocity was lower in both patient groups, but not significantly different from controls. Single peak, bell-shaped velocity profiles of the hand were preserved in all right hemispheric patients and in three out of five neglect patients. Most important, the velocity profiles of neglect patients to leftward targets did not differ significantly from those to targets in the right hemispace. In summary, we found evidence for general bradykinesia in neglect patients, but not for a direction-specific deficit in the control of hand velocity. We conclude that visual neglect induces characteristic changes in exploratory behavior, but not in the kinematics of goal-directed movements to objects in peripersonal space.     

Functional lateralization of the human premotor cortex during sequential movements

A neurological truism is that each side of the brain controls movements on the opposite side of the body. Yet some left hemisphere brain lesions cause bilateral impairment of complex motor function and/or ideomotor apraxia. We report that the left dorsal premotor cortex of normal right-handed people plays a fundamental role in sequential movement of both right and left hands. Subjects performed sequential finger movements during functional magnetic resonance imaging of the motor cortices. In right-handed subjects, the volume of activated dorsal premotor cortex showed a left hemispheric predominance during hand movements. We suggest that the observed left premotor dominance contributes to the lateralization found in lesion studies.     

Activations of "motor" and other non-language structures during sentence comprehension

In this paper we report the results of an experiment in which subjects read syntactically unambiguous and ambiguous sentences which were disambiguated after several words to the less likely possibility. Understanding such sentences involves building an initial structure, inhibiting the non-preferred structure, detecting that later input is incompatible with the initial structure, and reactivating the alternative structure. The ambiguous sentences activated four areas more than the unambiguous sentences. These areas are the left inferior frontal gyrus (IFG), the right basal ganglia (BG), the right posterior dorsal cerebellum (CB) and the left median superior frontal gyrus (SFG). The left IFG is normally activated when syntactic processing complexity is increased and probably supports that function in the current study as well. We discuss four hypotheses concerning how these areas may support comprehension of syntactically ambiguous sentences. (1) The left IFG, right CB and BG could support articulatory rehearsal used to support the processing of ambiguous sentences. This seems unlikely since the activation pattern associated with articulatory rehearsal in other studies is not similar to that seen here. (2) The CB acts as an error detector in motor processing. Error detection is important for recognizing that the wrong sentence structure has been chosen initially. (3) The BG acts to select and sequence movements in the motor domain and in cognitive domains may serve to inhibit competing and completed plans which is not unlike inhibiting the initially non-preferred structure or "unchoosing" the initial choice when incompatible syntactic input is received. (4) The left median SFG is relevant for the evaluation of plausibility. Evaluating the plausibility of the two possibilities provides an important basis for choosing between them. The notion of the use of domain general cognitive processes to support a linguistic process is in line with recent suggestions that the a given area may subserve a specific cognitive task because it carries out an appropriate sort of computation rather than because it supports a specific cognitive domain.     

Intermodal sensory image generation: An fMRI analysis

Although both imagery and perception may be related to more than one sensory input, and information coming from different sensory channels is often integrated in a unique mental representation, most recent neuroimaging literature has focused on visual imaging. Contrasting results have been obtained concerning the sharing of the same mechanisms by visual perception and visual imagery, in part due to assessment techniques and to interindividual variability in brain activation. In recent years, an increasing number of researchers have adopted novel neuroimaging techniques in order to investigate intermodal connections in mental imagery and have reported a high degree of interaction between mental imagery and other cognitive functions. In the present study the specific nature of mental imagery was investigated by means of fMRI on a more extensive set of perceptual experiences (shapes, sounds, touches, odours, flavours, self‐perceived movements, and internal sensations). Results show that the left middle‐inferior temporal area is recruited by mental imagery for all modalities investigated and not only for the visual one, while parietal and prefrontal areas exhibit a more heterogeneous pattern of activation across modalities. The prominent left lateralisation observed for almost all the conditions suggests that verbal cues affect the processes underlying the generation of images.     

Effects of motor intention on the perception of somatosensory events: a behavioural and functional magnetic resonance imaging study

The intention to execute a movement can modulate our perception of sensory events, and this modulation is observed ahead of both ocular and upper limb movements. However, theoretical accounts of these effects, and also the empirical data, are often contradictory. Accounts of "active touch", and the premotor theory of attention, have emphasized how movement intention leads to enhanced perceptual processing at the target of a movement, or on the to-be-moved effector. By contrast, recent theories of motor control emphasize how internal "forward" model (FM) estimates may be used to cancel or attenuate sensory signals that arise as a result of self-generated movements. We used behavioural and functional brain imaging (functional magnetic resonance imaging, fMRI) to investigate how perception of a somatosensory stimulus differed according to whether it was delivered to a hand that was about to execute a reaching movement or the alternative, nonmoving, hand. The results of our study demonstrate that a somatosensory stimulus delivered to a hand that is being prepared for movement is perceived to have occurred later than when that same stimulus is delivered to a nonmoving hand. This result indicates that it takes longer for a tactile stimulus to be detected when it is delivered to a moving limb and may correspond to a change in perceptual threshold. Our behavioural results are paralleled by the results of our fMRI study that demonstrated that there were significantly reduced blood-oxygen-level-dependent (BOLD) responses within the parietal operculum and insula following somatosensory stimulation of the hand being prepared for movement, compared to when an identical stimulus was delivered to a nonmoving hand. These findings are consistent with the prediction of FM accounts of motor control that postulate that central sensory suppression of somatosensation accompanies self-generated limb movements, and with previous reports indicating that effects of sensory suppression are observed in higher order somatosensory regions.     

When left is "right". Motor fluency shapes abstract concepts

Right- and left-handers implicitly associate positive ideas like "goodness" and "honesty" more strongly with their dominant side of space, the side on which they can act more fluently, and negative ideas more strongly with their nondominant side. Here we show that right-handers' tendency to associate "good" with "right" and "bad" with "left" can be reversed as a result of both long- and short-term changes in motor fluency. Among patients who were right-handed prior to unilateral stroke, those with disabled left hands associated "good" with "right," but those with disabled right hands associated "good" with "left," as natural left-handers do. A similar pattern was found in healthy right-handers whose right or left hand was temporarily handicapped in the laboratory. Even a few minutes of acting more fluently with the left hand can change right-handers' implicit associations between space and emotional valence, causing a reversal of their usual judgments. Motor experience plays a causal role in shaping abstract thought.     

Recognition and mental manipulation of body parts dissociate in locked-in syndrome

Several lines of evidence demonstrate that the motor system is involved in motor simulation of actions, but some uncertainty exists about the consequences of lesions of descending motor pathways on mental imagery tasks. Moreover, recent findings suggest that the motor system could also have a role in recognition of body parts. To address these issues in the present study we assessed patients with a complete damage of descending motor pathways (locked-in syndrome, LIS) on the hand laterality task, requiring subjects to decide whether a hand stimulus in a given spatial orientation represents a left or a right hand. LIS patients were less accurate than healthy controls in judging hand laterality; more importantly, LIS patients’ performance was modulated by spatial orientation of hand stimuli whereas it was not affected by biomechanical constraints. These findings demonstrate a dissociation between spared hand recognition and impaired access to action simulation processes in LIS patients.     

Manual localization of lateralized visual targets

The effects of visual field, responding limb and extrapersonal space on the ability to localize visual targets using slow positioning movements of the arm were examined. Special contact lenses were used to lateralize visual information and to make comparisons with localization under monocular control conditions. Subjects made slow positioning movements to place a cursor directly beneath target lights. They saw target lights but not the moving limb during the trial. For directional error, results indicated that subjects were more accurate localizing targets lateralized to the right hemisphere than targets lateralized to the left hemisphere, indicating right hemisphere superiority for localization of visual targets in grasping space. Localization performance was significantly better with the right hand than the left hand. the left hand demonstrated a directional bias to the right of the targets. Responding hand and visual field did not interact. Finally, contrary to subjects' awareness and verbal reports, target localization was not less accurate in lens than in monocular control conditions. This was true for both amplitude and directional error. This is consistent with other studies where visual information about limb position is not available.     

The Influence of Motor Imagery on Postural Sway: Differential Effects of Type of Body Movement and Person Perspective

The present study examined the differential effects of kinesthetic imagery (first person perspective) and visual imagery (third person perspective) on postural sway during quiet standing. Based on an embodied cognition perspective, the authors predicted that kinesthetic imagery would lead to activations in movement-relevant motor systems to a greater degree than visual imagery. This prediction was tested among 30 participants who imagined various motor activities from different visual perspectives while standing on a strain gauge plate. The results showed that kinesthetic imagery of lower body movements, but not of upper body movements, had clear effects on postural parameters (sway path length and frequency contents of sway). Visual imagery, in contrast, had no reliable effects on postural activity. We also found that postural effects were not affected by the vividness of imagery. The results suggest that during kinesthetic motor imagery participants partially simulated (re-activated) the imagined movements, leading to unintentional postural adjustments. These findings are consistent with an embodied cognition perspective on motor imagery.