Scott H. Frey

Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp

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.

A Common Network in the Left Cerebral Hemisphere Represents Planning of Tool Use Pantomimes and Familiar Intransitive Gestures at the Hand-Independent Level

Evidence from neuropsychology and neuroimaging implicates parietal and frontal areas of the left cerebral hemisphere in the representation of skills involving the use of tools and other artifacts. On the basis of neuropsychological data, it has been claimed that 1) independent mechanisms within the left hemisphere may support the representation of these skills (transitive actions) versus meaningful gestures that do not involve manipulating objects (intransitive actions), and 2) both cerebral hemispheres may participate in the representation of intransitive gestures. Functional magnetic resonance imaging was used to test these hypotheses in 12 healthy adults while they planned and executed tool use pantomimes or intransitive gestures with their dominant right (Exp. 1) or nondominant left (Exp. 2) hands. Even when linguistic processing demands were controlled, planning either type of action was associated with asymmetrical increases in the same regions of left parietal (the intraparietal sulcus, supramarginal gyrus, and caudal superior parietal lobule) and dorsal premotor cortices. Effects were greater for tool use pantomimes, but only when the right hand was involved. Neither group nor individual analyses revealed evidence for greater bilateral activity during intransitive gesture planning. In summary, at the hand-independent level, transitive and intransitive actions are represented in a common, left-lateralized praxis network.

Tool use, communicative gesture and cerebral asymmetries in the modern human brain

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 actors 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.

Neural representations involved in observed, imagined, and imitated actions are dissociable and hierarchically organized.

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.

Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool

Humans display a remarkable capacity to use tools instead of their biological effectors. Yet, little is known about the mechanisms that support these behaviors. Here, participants learned to grasp objects, appearing in a variety of orientations, with a novel, handheld mechanical tool. Following training, psychophysical functions relating grip preferences (i.e., pronated vs. supinated) to stimulus orientations indicate a reliance on distinct, effector-specific internal representations when planning grasping actions on the basis of the tool versus the hands. Accompanying fMRI data show that grip planning in both hand and tool conditions was associated with similar increases in activity within the same regions of the anterior intraparietal and caudal ventral premotor cortices, a putative homologue of the macaque anterior intraparietal–ventral premotor (area F5) “grasp circuit.” These findings suggest that tool use is supported by effector-specific representations of grasping with the tool that are functionally independent of previously existing representations of the hand and yet occur within the same parieto-frontal regions involved in manual prehension. These levels of representation are critical for accurate planning and execution of actions in a manner that is sensitive to the respective properties of these effectors. These effector-specific representations likely coexist with effector-independent representations. The latter were recently reported in macaque F5 [Umiltà, M. A., Escola, L., Intskirveli, I., Grammont, F., Rochat, M., Caruana, F., et al. When pliers become fingers in the monkey motor system. Proceedings of the National Academy of Sciences, U.S.A., 105, 2209–2213, 2008] and appear to be established by tool use training through modification of existing representations of grasping with the hand. These more abstract levels of representation may facilitate the transfer of skills between hand and tool.

Tool use and the distalization of the end-effector

We review recent neurophysiological data from macaques and humans suggesting that the use of tools extends the internal representation of the actor’s hand, and relate it to our modeling of the visual control of grasping. We introduce the idea that, in addition to extending the body schema to incorporate the tool, tool use involves distalization of the end-effector from hand to tool. Different tools extend the body schema in different ways, with a displaced visual target and a novel, task-specific processing of haptic feedback to the hand. This distalization is critical in order to exploit the unique functional capacities engendered by complex tools.

A Dissociation between the Representation of Tool-use Skills and Hand Dominance: Insights from Left- and Right-handed Callosotomy Patients

The overwhelming majority of evidence indicates that the left cerebral hemisphere of right-handed humans is dominant both for manual control and the representation of acquired skills, including tool use. It is, however, unclear whether these functions involve common or dissociable mechanisms. Here we demonstrate that the disconnected left hemispheres of both right- and left-handed split-brain patients are specialized for representing acquired tool-use skills. When required to pantomime actions associated with familiar tools (Experiment 2), both patients show a right-hand (left hemisphere) advantage in response to tool names, pictures, and actual objects. Accuracy decreases as stimuli become increasingly symbolic when using the left hand (right hemisphere). Tested in isolation with lateralized pictures (Experiment 3), each patients left hemisphere demonstrates a significant advantage over the right hemisphere for pantomiming tool-use actions with the contralateral hand. The fact that this asymmetry occurs even in a left-handed patient suggests that the left hemisphere specialization for representing praxis skills can be dissociated from mechanisms involved in hand dominance located in the right hemisphere. This effect is not attributable to differences at the conceptual level, as the left and right hemispheres are equally and highly competent at associating tools with observed pantomimes (Experiment 4).

Handedness-dependent and –independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning

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.

Atypical lateralization of language predicts cerebral asymmetries in parietal gesture representations

Humans typically show left-hemisphere dominance both for language and manual gestures. If this reflects a dependence of these behaviors on a common cerebral specialization, then healthy left-handers with atypical organization of language should show a similar pattern for gesture. Consistent with this hypothesis, we report fMRI data indicating that sinistrals (5/15) with bilateral, or right-lateralized, language representations in inferior frontal cortex exhibit a similar atypical pattern in inferior parietal representations of familiar gestures.

Neurological Principles and Rehabilitation of Action Disorders: Computation, Anatomy, and Physiology (CAP) Model

This chapter outlines the basic computational, anatomical, and physiological (CAP) principles underlying upper-limb actions, such as reaching for a cup and grasping it or picking up a key, inserting it into a lock, and turning it.