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Biomedical subjects

Angela Sirigu

Publications and source records attributed to Angela Sirigu.

At least 19 recordsLinked to original sources

Mapping phantom movement representations in the motor cortex of amputees.

Limb amputation results in plasticity of connections between the brain and muscles, with the cortical motor representation of the missing limb seemingly shrinking, to the presumed benefit of remaining body parts that have cortical representations adjacent to the now-missing limb. Surprisingly, the corresponding perceptual representation does not suffer a similar fate but instead persists as a phantom limb endowed with sensory and motor qualities. How can cortical reorganization after amputation be reconciled with the maintenance of a motor representation of the phantom limb in the brain? In an attempt to answer this question we explored the relationship between the cortical representation of the remaining arm muscles and that of phantom movements. Using transcranial magnetic stimulation (TMS) we systematically mapped phantom movement perceptions while simultaneously recording stump muscle activity in three above-elbow amputees. TMS elicited sensations of movement in the phantom hand when applied over the presumed hand area of the motor cortex. In one subject the amplitude of the perceived movement was positively correlated with the intensity of stimulation. Interestingly, phantom limb movements that the patient could not produce voluntarily were easily triggered by TMS, suggesting that the inability to voluntarily move the phantom is not equivalent to a loss of the corresponding movement representation. We suggest that hand movement representations survive in the reorganized motor area of amputees even when these cannot be directly accessed. The activation of these representations is probably necessary for the experience of phantom movement.

Amputation Stumps↗

Persistent hand motor commands in the amputees' brain.

The loss of a limb leads to sensorimotor modifications that are frequently accompanied by the vivid experience that the missing limb is still present, and that it can be moved at will. Furthermore, amputees can clearly distinguish between phantom movements of the fingers and of more proximal joints, like movements of the elbow. This phenomenon raises the question of whether these specific phantom movement experiences are translated into differentiated activity within the remaining muscles. We recorded stump muscle activity when above-elbow amputees voluntarily moved their phantom limb. Voluntary movements of the phantom hand triggered specific patterns of stump muscle activity, which differed from activity recorded in the same muscle groups during movements of the proximal limb. This result indicates that the brain's motor areas can be differentially activated according to the phantom movement the patient intends to perform, and suggests that hand motor commands are preserved after amputation. To further understand the interaction between central commands and sensory feedback in the perception of phantom movement we also measured stump muscle EMG activity in an amputee experiencing a frozen phantom limb, and in three below-elbow amputees with vivid phantom movements after inducing an ischaemic block. Failed attempts to move the paralysed phantom limb always resulted in the same EMG pattern, no matter what type of phantom movement was attempted, while ischaemic nerve block reduced or eliminated the ability to voluntarily move the phantom limb and produced a dramatic reduction in the amplitude of stump muscle EMG activity. Our data suggest that the experience of phantom hand movement involves the activation of hand motor commands. We propose that preserved hand movement representations re-target the stump muscles to express themselves and that when these representations are voluntarily accessible they can instruct the remaining muscles to move in such a way as if the limb is still there.

Amputation Stumps↗

How we interact with objects: learning from brain lesions.

Motor deficits are the most common outcome of brain damage. Although a large part of such disturbances arises from loss of elementary sensorimotor functions, several syndromes cannot be explained purely on these bases. In this article, we briefly describe higher-order motor impairments, with specific attention to the characteristic ability of the human hand to interact with objects and tools. Disruption of this motor skill at several independent levels is used to outline a comprehensive model, in which various current proposals for a modular organization of hand-object interactions can be integrated. In this model, cortical mechanisms related to object interaction are independent from representations of the semantic features of objects.

Brain Injuries↗

Sense of motor effort in patients with schizophrenia.

We tested the hypothesis suggesting that internally generated signals related to motor command would not be processed in schizophrenic patients with first rank symptoms (FRS). To address this question, we investigated an aspect of the efference copy not yet investigated in schizophrenia, namely its implication in sensation of effort. We assessed sensation of effort in healthy subjects (n = 17) and in schizophrenic patients with (n = 6) and without (n = 11) FRS using two tasks. In the first, subjects were required to produce isometric target-forces under visual control with one hand (reference hand), and then, without external feedback, to transfer the same effort to the other hand (matched hand). In the second, subjects had to produce force impulses whose magnitude was proportional to numerical values. The results of the first experiment showed that all subjects could maintain a significant relationship between the force exerted by the reference hand and the force exerted by the matching hand. Results from the second experiment indicated that the strength of the relationship between desired efforts and achieved peak forces was lower in both patient groups compared to controls. Taken together our findings indicate that one component of efference copy--its implication in sensing achieved effort--is preserved in schizophrenia. We propose that schizophrenic patients and particularly those with FRS are impaired in the ability to represent intended effort. The detection threshold of centrally generated signals by the higher order level of the motor representation may be abnormally high in these patients.

Adult↗

Regret and its avoidance: a neuroimaging study of choice behavior.

Human decisions can be shaped by predictions of emotions that ensue after choosing advantageously or disadvantageously. Indeed, anticipating regret is a powerful predictor of future choices. We measured brain activity using functional magnetic resonance imaging (fMRI) while subjects selected between two gambles wherein regret was induced by providing information about the outcome of the unchosen gamble. Increasing regret enhanced activity in the medial orbitofrontal region, the anterior cingulate cortex and the hippocampus. Notably, across the experiment, subjects became increasingly regret-aversive, a cumulative effect reflected in enhanced activity within medial orbitofrontal cortex and amygdala. This pattern of activity reoccurred just before making a choice, suggesting that the same neural circuitry mediates direct experience of regret and its anticipation. These results demonstrate that medial orbitofrontal cortex modulates the gain of adaptive emotions in a manner that may provide a substrate for the influence of high-level emotions on decision making.

Adult↗

Memory and action: an experimental study on normal subjects and schizophrenic patients.

Psychologists have shown that recall of sentences describing previously performed actions is enhanced compared to recall of heard-only action-phrases (enactment effect). One interpretation of this effect argues that subjects benefit from a multi-modal encoding where movement plays a major role. In line with this motor account, it is conceivable that the beneficial effect of enactment might rely, at least in part, on procedural learning, thus tapping more directly implicit memory functions. Neuropsychological observations support this hypothesis, as shown by the fact that the enactment effect is quite insensitive to perturbations affecting declarative memories. i.e. Alzheimer disease. Memory for subject performed tasks in patients with Korsakoff syndrome. The present study attempts to evaluate whether pure motor activity is sufficient to guarantee the described memory facilitation or alternatively, whether first-person experience in carrying out the action (i.e. true enactment) would be required. To this purpose, in a first experiment on healthy subjects, we tested whether sentence meaning and content of the executed action should match in order to produce facilitation in recall of enacted action-phrases. In a second experiment, we explored whether the enactment effect is present in patients suffering from psychiatric disorders supposed to spare procedural memory but to alter action awareness (e.g. schizophrenia). We show that better recall for action phrases is found only when the motor component is a true enactment of verbal material. Moreover, this effect is nearly lost in schizophrenia. This latter result, on the one hand, queries the automatic/implicit nature of the enactment effect and supports the role of the experience of having performed the action in the first-person. On the other hand, it questions the nature of the memory impairments detected in schizophrenia.

Adolescent↗

A specific role for efferent information in self-recognition.

We investigated the specific contribution of efferent information in a self-recognition task. Subjects experienced a passive extension of the right index finger, either as an effect of moving their left hand via a lever ('self-generated action'), or imposed externally by the experimenter ('externally-generated action'). The visual feedback was manipulated so that subjects saw either their own right hand ('view own hand' condition) or someone else's right hand ('view other's hand' condition) during the passive extension of the index finger. Both hands were covered with identical gloves, so that discrimination on the basis of morphological differences was not possible. Participants judged whether the right hand they saw was theirs or not. Self-recognition was significantly more accurate when subjects were themselves the authors of the action, even though visual and proprioceptive information always specified the same posture, and despite the fact that subjects judged the effect and not the action per se. When the passive displacement of the participants right index finger was externally generated, and only afferent information was available, self-recognition performance dropped to near-chance levels. Differences in performance across conditions reflect the distinctive contribution of efferent information to self-recognition, and argue against a dominant role of proprioception in self-recognition.

Adult↗

Motor activation prior to observation of a predicted movement.

Previous research has shown that some of the same motor regions are activated both when performing and when observing a movement. Here we demonstrate in human subjects that such motor activity also occurs prior to observing someone else's action. This suggests that the mere knowledge of an upcoming movement is sufficient to excite one's own motor system, enabling people to anticipate, rather than react to, others' actions.

Electroencephalography↗

Perception of dynamic action in patients with schizophrenia.

Neuropsychological studies have revealed that schizophrenic (SZ) patients have severe impairments in the cognitive integration of static and moving perceptual stimuli. Research on knowledge structures has shown that sequences of continuous actions are represented in memory as clusters of goal-directed events in a hierarchical manner. In the present study, we investigated the ability to segment familiar sequences of dynamic goal-directed actions into small and large meaningful units in a group of patients with schizophrenia (N = 16) and a group of healthy control subjects (N = 17). While viewing two videotaped movies, participants were requested to detect the transitions between component events at both low and high levels of the action categorical structure. Both groups detected significantly more events under the small-oriented condition as compared to the large-oriented condition. Differently from normal controls, patients recalled the event scenes in a detailed and fragmentary manner and showed considerable difficulties in detecting large action units. Moreover, low performance on action boundary detection significantly correlated with higher levels of disorganisation symptoms in patients with schizophrenia. A defective conceptual organisation of perceptive action knowledge would help to explain the severe everyday difficulties of these patients both in monitoring their own actions and in understanding others' intentions.

Adult↗

Spatial coding of the predicted impact location of a looming object.

Avoiding or intercepting looming objects implies a precise estimate of both time until contact and impact location. In natural situations, extrapolating a movement trajectory relative to some egocentric landmark requires taking into account variations in retinal input associated with moment-to-moment changes in body posture. Here, human observers predicted the impact location on their face of an approaching stimulus mounted on a robotic arm, while we systematically manipulated the relation between eye, head, and trunk orientation. The projected impact point on the observer's face was estimated most accurately when the target originated from a location aligned with both the head and eye axes. Eccentric targets with respect to either axis resulted in a systematic perceptual bias ipsilateral to the trajectory's origin. We conclude that (1) predicting the impact point of a looming target requires combining retinal information with eye position information, (2) that this computation is accomplished accurately for some, but not all, possible combinations of these cues, (3) that the representation of looming trajectories is not formed in a single, canonical reference frame, and (4) that the observed perceptual biases could reflect an automatic adaptation for interceptive/defensive actions within near peripersonal space.

Adult↗

The involvement of the orbitofrontal cortex in the experience of regret.

Facing the consequence of a decision we made can trigger emotions like satisfaction, relief, or regret, which reflect our assessment of what was gained as compared to what would have been gained by making a different decision. These emotions are mediated by a cognitive process known as counterfactual thinking. By manipulating a simple gambling task, we characterized a subject's choices in terms of their anticipated and actual emotional impact. Normal subjects reported emotional responses consistent with counterfactual thinking; they chose to minimize future regret and learned from their emotional experience. Patients with orbitofrontal cortical lesions, however, did not report regret or anticipate negative consequences of their choices. The orbitofrontal cortex has a fundamental role in mediating the experience of regret.

Adult↗

Altered awareness of voluntary action after damage to the parietal cortex.

A central question in the study of human behavior is the origin of willed action. EEG recordings of surface brain activity from human subjects performing a self-initiated movement show that the subjective experience of wanting to move follows, rather than precedes, the 'readiness potential'--an electrophysiological mark of motor preparation. This raises the issue of how conscious experience of willed action is generated. Here we show that patients with parietal lesions can report when they started moving, but not when they first became aware of their intention to move. This stands in contrast with the performance of cerebellar patients who behaved as normal subjects. We thus propose that when a movement is planned, activity in the parietal cortex, as part of a cortico-cortical sensorimotor processing loop, generates a predictive internal model of the upcoming movement. This model might form the neural correlate of motor awareness.

Adult↗

Left and right hand recognition in upper limb amputees.

Previous research suggests a close similarity in brain activity between mental simulation of a movement and its real counterpart. To explore this similarity, we aimed to assess whether imagery is affected by the loss of a limb or of its motor skills. We examined the performance of 16 adult, upper limb amputees (and age-matched controls) in a left/right hand judgement task that implicitly requires motor imagery. The experimental group included subjects who had suffered the amputation of the dominant or the non-dominant limb. Although responding well above chance, amputees as a group were slower and less accurate than controls. Nevertheless, their response pattern was similar to that of controls, namely slower response times and more errors for stimuli depicting hands in unnatural orientations, i.e. postures difficult to reach with a real movement. Interestingly, for all stimuli, amputees' performance was strongly affected by the side of limb loss: subjects who underwent amputation of their preferred limb made more errors and required greater latencies to respond as compared with amputees of the non-dominant limb. In a further analysis we observed that the habit of wearing an aesthetic prosthesis significantly interfered with the ability to judge the corresponding hand. Our data lead to three main conclusions: (i) loss of a single limb per se does not prevent motor imagery but it significantly enhances its difficulty; (ii) these subjects apparently perform the hand recognition task using a strategy in which they initially mentally simulate movements of their dominant limb; (iii) wearing a prosthesis, devoid of any motor function, seems to interfere with motor imagery, consistent with the view that only 'tools' can be incorporated in a dynamic body schema.

Adult↗

Action prediction in the cerebellum and in the parietal lobe.

The ability of the central nervous system to predict motor behaviour is a central issue in experimental and computational studies of motor control. The parietal cortex and the cerebellum have been proposed to play a role in sensorimotor prediction. Here we discuss the roles of these two brain regions in various aspects of sensorimotor prediction according to results of recent empirical studies using a variety of techniques including electrophysiology, psychophysics, functional neuroimaging and the investigation of neurological patients.

Animals↗

Cognitive representations of hand posture in ideomotor apraxia.

Ideomotor apraxia (IM) is a disorder of skilled action characterized by spatiotemporal errors in pantomiming object use and in using objects. Recent evidence suggests that at least some patients with IM may exhibit particular deficits in forming hand configurations appropriate for object use. Sirigu et al. [Cortex 31 (1995) 41] reported an apraxic who positioned her hand inappropriately when attempting to use objects in accordance with stored knowledge of object-specific manipulation, but in reaching tasks could grasp the same objects appropriately in response to their structure. To this point, however, apraxics' ability to respond to functional and structural attributes of objects has not been empirically assessed. We investigated the hypothesis that patients with IM (n=9) due to left inferior parietal damage would be impaired in producing and recognizing hand postures associated with familiar objects, indicating deficient memorial representations for object-specific hand postures. In contrast, we predicted relatively unimpaired ability to produce and recognize appropriate hand postures with novel objects, indicating integrity of "on line" spatiomotor procedures coding hand position in response to object structure. Apraxics' performance was contrasted with 10 healthy controls and 8 brain-lesioned non-apraxics. Consistent with our predictions, the apraxics responded abnormally with familiar objects but normally in recognizing hand postures appropriate for novel objects. In addition, performance with objects calling for a prehensile response (pinch or clench) was superior to that with objects evoking a non-prehensile response (palm or poke). These data suggest degradation of inferior parietally-mediated representations of the precise hand postures associated with familiar objects. Furthermore, they are consistent with possible over-reliance upon dorsal system procedures for calculating precision and power grip in response to object structure.

Aged↗

Perception of action boundaries in patients with frontal lobe damage.

The prefrontal cortex is known to be involved in action planning and in controlling behaviour. Neuropsychological evidence also supports the idea that the prefrontal cortex is generally involved in processing complex events, such as action knowledge. Actions are represented in memory as sequences of goal-directed discrete events. Complex events can be divided into discrete smaller units and organised in a hierarchical manner. The aim of the present study was to investigate the ability of 9 patients with prefrontal lesion and 12 healthy controls to parse action sequences into meaningful events. Subjects were requested to detect the transitions between events under three different orientation instructions: (1) spontaneous; (2) small events; and (3) large event. Both normal subjects and patients identified significantly more events under the small-oriented condition. However, contrary to normal controls (NCs), patients with prefrontal damage showed considerable difficulties in detecting large event units than small event units. These results strongly suggest that prefrontal cortex is specifically involved in parsing and recognising clusters of action sequences. These findings also show that the way in which instructions orient subjects' attention, has an effect on how action information is encoded and represented in memory.

Adult↗

Being the agent: memory for action events.

Whoever paid the bill at the restaurant last night, will clearly remember doing it. Independently from the type of action, it is a common experience that being the agent provides a special strength to our memories. Even if it is generally agreed that personal memories (episodic memory) rely on separate neural substrates with respect to general knowledge (semantic memory), little is known on the nature of the link between memory and the sense of agency. In the present paper, we review results from two experiments investigating the effects of agency on both explicit and implicit memory traces. Performance of normal subjects is compared to that of schizophrenic patients in order to explore the role of awareness of action on memory. It is proposed that reliable first-person information is necessary to create a stable and coherent motor memory trace.

Adult↗