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Determining the brain adaptations that underlie complex tool-use skills is an important component in understanding the physiological bases of human material culture. It is argued here that the ways in which humans skilfully use tools and other manipulable artefacts is possible owing to adaptations that integrate sensory-motor and cognitive processes. Data from brain-injured patients and functional neuroimaging studies suggest that the left cerebral hemisphere, particularly the left parietal cortex, of modern humans is specialized for this purpose. This brain area integrates dynamically representations that are computed in a distributed network of regions, several of which are also left-lateralized. Depending on the nature of the task, these may include conceptual knowledge about objects and their functions, the actor's goals and intentions, and interpretations of task demands. The result is the formation of a praxis representation that is appropriate for the prevailing task context. Recent evidence is presented that this network is organized similarly in the right- and left-handed individuals, and participates in the representation of both familiar tool-use skills and communicative gestures. This shared brain mechanism may reflect common origins of the human specializations for complex tool use and language.

The fact that action observation, motor imagery and execution are associated with partially overlapping increases in parieto-frontal areas has been interpreted as evidence for reliance of these behaviors on a common system of motor representations. However, studies that include all three conditions within a single paradigm are rare, and consequently, there is a dearth of knowledge concerning the distinct mechanisms involved in these functions. Here we report key differences in neural representations subserving observation, imagery, and synchronous imitation of a repetitive bimanual finger-tapping task using fMRI under conditions in which visual stimulation is carefully controlled. Relative to rest, observation, imagery, and synchronous imitation are all associated with widespread increases in cortical activity. Importantly, when effects of visual stimulation are properly controlled, each of these conditions is found to have its own unique neural signature. Relative to observation or imagery, synchronous imitation shows increased bilateral activity along the central sulcus (extending into precentral and postcentral gyri), in the cerebellum, supplementary motor area (SMA), parietal operculum, and several motor-related subcortical areas. No areas show greater increases for imagery vs. synchronous imitation; however, relative to synchronous imitation, observation is associated with greater increases in caudal SMA activity than synchronous imitation. Compared to observation, imagery increases activation in pre-SMA and left inferior frontal cortex, while no areas show the inverse effect. Region-of-interest (ROI) analyses reveal that areas involved in bimanual open-loop movements respond most to synchronous imitation (primary sensorimotor, classic SMA, and cerebellum), and less vigorously to imagery and observation. The differential activity between conditions suggests an alternative hierarchical model in which these behaviors all rely on partially independent mechanisms. ► Compared neural representations for observation, imagery, and imitation with fMRI. ► Controlled visual stimulation reveals a hierarchical organization. ► Imitation > imagery or observation in sensorimotor cortex, SMA and cerebellum. ► Imagery > observation in pre-SMA, cerebellum, left IFg, insula, and cingulate Gyrus. ► Observation > imitation in caudalmost SMA.

Animal models reveal that deafferenting forelimb injuries precipitate reorganization in both contralateral and ipsilateral somatosensory cortices. The functional significance and duration of these effects are unknown, and it is unclear whether they also occur in injured humans. We delivered cutaneous stimulation during functional magnetic resonance imaging (fMRI) to map the sensory cortical representation of the intact hand and lower face in a group of chronic, unilateral, upper extremity amputees (N = 19) and healthy matched controls (N = 29). Amputees exhibited greater activity than controls within the deafferented former sensory hand territory (S1f) during stimulation of the intact hand, but not of the lower face. Despite this cortical reorganization, amputees did not differ from controls in tactile acuity on their intact hands. S1f responses during hand stimulation were unrelated to tactile acuity, pain, prosthesis usage, or time since amputation. These effects appeared specific to the deafferented somatosensory modality, as fMRI visual mapping paradigm failed to detect any differences between groups. We conclude that S1f becomes responsive to cutaneous stimulation of the intact hand of amputees, and that this modality-specific reorganizational change persists for many years, if not indefinitely. The functional relevance of these changes, if any, remains unknown.

Adaptive motor behavior requires efficient error detection and correction. The posterior parietal cortex is critical for on-line control of reach-to-grasp movements. Here we show a causal relationship between disruption of cortical activity within the anterior intraparietal sulcus (aIPS) by transcranial magnetic stimulation (TMS) and disruption of goal-directed prehensile actions (either grip size or forearm rotation, depending on the task goal, with reaching preserved in either case). Deficits were elicited by applying TMS within 65 ms after object perturbation, which attributes a rapid control process on the basis of visual feedback to aIPS. No aperture deficits were produced when TMS was applied to a more caudal region within the intraparietal sulcus, to the parieto-occipital complex (putative V6, V6A) or to the hand area of primary motor cortex. We contend that aIPS is critical for dynamic error detection during goal-dependent reach-to-grasp action that is visually guided.

Affordance perception is critical to adaptive behavior. It comprises the ability to evaluate whether the environment and the actor's capabilities enable particular actions. It remains unclear how brain damage and its behavioral sequela impact this ability. Two affordance based judgment tasks were applied in healthy young adults that were adapted for prospective diagnostic purposes in patients. In addition to the commonly analyzed error-rate we included response times and accuracy measures based on a detection theory approach. Moreover, a manipulation was added intended to determine the effectiveness of feedback-based learning. We further applied control tasks that consider whether errors in affordance perception can be explained by errors in perception. Participants responded yes or no to decide prospectively if a given setting would afford a particular action. In study1, 27 participants judged whether their hand would fit through a given aperture (adapted from Ishak et al., 2008). In study2, 19 participants judged whether objects are reachable [adapted from Gabbard et al. (2005)]. For both studies two sessions were administered. In the first session all participants solved the judgment-task without executing the action. In the second session (feedback manipulation), half of the participants were allowed to first judge and then perform the task for each trial (reach forward and touch the object, or fitting the hand into the aperture). Judgments were slowest and errors most frequent for openings or distances close to the individual's actual physical limits. With more extreme settings accuracy increased and responses became faster. Importantly, we found an advantageous effect of feedback on performance in both tasks suggesting that affordance perception is rapidly trainable. Further, the aperture task demonstrated that feedback experienced with one hand can transfer to the other. This may have important implications for rehabilitation.

The ability to judge accurately whether or not an action can be accomplished successfully is critical for selecting appropriate response options that enable adaptive behaviors. Such affordance judgments are thought to rely on the perceived fit between environmental properties and knowledge of one's current physical capabilities. Little, however, is currently known about the ability of individuals to judge their own affordances following a stroke, or about the underlying neural mechanisms involved. To address these issues, we employed a signal detection approach to investigate the impact of left or right hemisphere injuries on judgments of whether a visual object was located within reach while remaining still (i.e., reachability). Regarding perceptual sensitivity and accuracy in judging reachability, there were no significant group differences between healthy controls ( N = 29), right brain damaged (RBD, N = 17) and left brain damaged stroke patients (LBD, N = 17). However, while healthy controls and RBD patients demonstrated a negative response criterion and thus overestimated their reach capability, LBD patients' average response criterion converged to zero, indicating no judgment tendency. Critically, the LBD group's judgment tendency pattern is consistent with previous findings in this same sample on an affordance judgment task that required estimating whether the hand can fit through apertures (Randerath et al., 2018 ). Lesion analysis suggests that this loss of judgment tendency may be associated with damage to the left insula, the left parietal and middle temporal lobe. Based on these results, we propose that damage to the left ventro-dorsal stream disrupts the retrieval and processing of a stable criterion, leading to stronger reliance on intact on-line body-perceptive processes computed within the preserved bilateral dorsal network.

Empathy requires the ability to map the feelings of others onto our own nervous system. Until recently, there was no plausible mechanism to explain how such a mapping might occur. The discovery of mirror neurons, however, suggests that the nervous system is capable of mapping the observed actions of others onto the premotor cortex of the self, at least for reaching and grasping movements. Is there a mirroring system for emotive actions, such as facial expression? Subjects ( N = 15; all right-handed; eight men, seven women) watched movies of facial expressions (smile or frown) and hand movements (move index or middle finger) while brain activity was imaged using functional magnetic resonance imaging (fMRI). Subjects watched the movies under three different conditions: passive viewing, active imitation, and an active motor control. Subjects also performed a verb generation task to functionally identify language-processing areas. We found evidence for a common cortical imitation circuit for both face and hand imitation, consisting of Broca's area, bilateral dorsal and ventral premotor areas, right superior temporal gyrus (STG), supplementary motor area, posterior temporo-occipital cortex, and cerebellar areas. For faces, passive viewing led to significant activation in the right ventral premotor area, whereas imitation produced bilateral activation. This result is consistent with evidence for right hemisphere (RH) dominance for emotional processing, and suggests that there may be a right hemisphere mirroring system that could provide a neural substrate for empathy.

The processes underlying action planning are fundamental to adaptive behavior and can be influenced by recent motor experience. Here, we used a novel fMRI Repetition Suppression (RS) design to test the hypotheses that action planning unfolds more efficiently for successive actions made with the same hand. More efficient processing was predicted to correspond with both faster response times (RTs) to initiate actions and reduced fMRI activity levels — RS. Consistent with these predictions, we detected faster RTs for actions made with the same hand and accompanying fMRI-RS within bilateral posterior parietal cortex and right-lateralized parietal operculum. Within posterior parietal cortex, these RS effects were localized to intraparietal and superior parietal cortices. These same areas were more strongly activated for actions involving the contralateral hand. The findings provide compelling new evidence for the specification of action plans in hand-specific terms, and indicate that these processes are sensitive to recent motor history. Consistent with computational efficiency accounts of motor history effects, the findings are interpreted as evidence for comparatively more efficient processing underlying action planning when successive actions involve the same versus opposite hand. •Participants use either hand to manipulate real objects in the MRI scanner.•Successive actions with the same hand are more efficiently planned.•Reduced response times and fMRI Repetition Suppression co-occur.•Hand-specific planning involves bilateral posterior parietal cortex.

Hand loss can now be reversed through surgical transplantation years or decades after amputation. Remarkably, these patients come to use their new hand to skilfully grasp and manipulate objects. The brain mechanisms that make this possible are unknown. Here we test the hypothesis that the anterior intraparietal cortex (aIPC) – a multimodal region implicated in hand preshaping and error correction during grasping – plays a key role in this compensatory grasp control. Motion capture and fMRI are used to characterize hand kinematics and brain responses during visually guided grasping with a transplanted hand at 26 and 41 months post-transplant in patient DR, a former hand amputee of 13 years. Compared with matched controls, DR shows increasingly normal grasp kinematics paralleled by increasingly robust grasp-selective fMRI responses within the very same brain areas that show grasp-selectivity in controls, including the aIPC, premotor and cerebellar cortices. Paradoxically, over this same time DR exhibits significant limitations in basic sensory and motor functions, and persistent amputation-related functional reorganization of primary motor cortex. Movements of the non-transplanted hand positively activate the ipsilateral primary motor hand area – a functional marker of persistent interhemispheric amputation-related reorganization. Our data demonstrate for the first time that even after more than a decade of living as an amputee the normative functional brain organization governing the control of grasping can be restored. We propose that the aIPC and interconnected premotor and cerebellar cortices enable grasp normalization by compensating for the functional impact of reorganizational changes in primary sensorimotor cortex and targeting errors in regenerating peripheral nerves. •We provide the first functional brain data of grasping with a transplanted hand.•Normative grasp kinematics parallel normative grasp-selective fMRI responses.•Grasp recovers despite persistent low-level deficits and changes in motor cortex.•Grasp and its normative brain organization are restored after hand transplantation.

When planning grasping actions, right-handers show left-lateralized responses in the anterior intraparietal sulcus (aIPS) and ventral premotor cortex (vPMC), two areas that are also implicated in sensorimotor control of grasp. We investigated whether a similar cerebral asymmetry is evident in strongly left-handed individuals. Fourteen participants were trained to grasp an object appearing in a variety of orientations with their left and right hands and with a novel mechanical tool (operated with either hand). BOLD fMRI data were then acquired while they decided prospectively whether an over- or under-hand grip would be most comfortable for grasping the same stimulus set while remaining still. Behavioral performances were equivalent to those recorded previously in right-handers and indicated reliance on effector-specific internal representations. In left-handers, however, grip selection decisions for both sides (left, right) and effectors (hand, tool) were associated with bilateral increases in activity within aIPS and vPMC. A direct comparison between left- and right-handers did reveal equivalent increases in left vPMC regardless of hand dominance. By contrast, aIPS and right vPMC activity were dependent on handedness, showing greater activity in the motor-dominant hemisphere. Though showing bilateral increases in both left- and right-handers, greater increases in the motor dominant hemisphere were also detected in the caudal IPS (cIPS), superior parietal lobule (SPL) and dorsal premotor cortex (dPMC). These findings provide further evidence that regions involved in the sensorimotor control of grasp also participate in grasp planning, and that for certain areas hand dominance is a predictor of the cerebral organization of motor cognitive functions. ► Equivalent effector-specific grip selection behaviors for left- and right-handers ► Equivalent increases in left vPMC regardless of hand dominance ► Increased aIPS and right vPMC activity in the motor-dominant hemisphere ► Hand dominance predicts the cerebral organization of certain motor cognitive functions.