Emily S. Cross

Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach

According to Milner and Goodales theory of the two visual streams, the dorsal (action) stream controls actions in real-time, whereas the ventral (perceptual) stream stores longer-term information for object identification. By this account, the dorsal stream subserves actions carried out immediately. However, when a delay is required before the response, the ventral (perceptual) stream is recruited. Indeed, a neuroimaging study from our lab has found reactivation of an area within the ventral stream, the lateral occipital (LO) cortex, at the time of action even when no visual stimulus was present. To tease apart the contribution of specific areas within the dorsal and ventral streams to the online control of grasping under immediate and delayed conditions, we used transcranial magnetic stimulation (TMS) to the anterior intraparietal sulcus (aIPS) and to LO. We show that while TMS to aIPS affected grasp under both immediate and delayed conditions, TMS to LO influenced grasp only under delayed movement conditions. The effects of TMS were restricted to early movement kinematics (i.e. within 300 ms) due to the transient nature of TMS, which was always delivered simultaneous with movement onset. We discuss the implications of our findings in relation to interactions between the dorsal and ventral streams.

Dissociable substrates for body motion and physical experience in the human action observation network

Observation of human actions recruits a well‐defined network of brain regions, yet the purpose of this action observation network (AON) remains under debate. Some authors contend that this network has developed to respond specifically to observation of human actions. Conversely, others suggest that this network responds in a similar manner to actions prompted by human and non‐human cues, and that one’s familiarity with the action is the critical factor that drives this network. Previous studies investigating human and non‐human action cues often confound novelty and stimulus form. Here, we used a dance‐learning paradigm to assess AON activity during observation of trained and untrained dance cues where a human model was present or absent. Results show that individual components of the AON respond differently to the human form and to dance training. The bilateral superior temporal cortex responds preferentially to videos with a human present, regardless of training experience. Conversely, the right ventral premotor cortex responds more strongly when observing sequences that had been trained, regardless of the presence of a human. Our findings suggest that the AON comprises separate and dissociable components for motor planning and observing other people’s actions.

Neural substrates of contextual interference during motor learning support a model of active preparation

When individuals acquire new skills, initial performance is typically better and tasks are judged to be easier when the tasks are segregated and practiced by block, compared to when different tasks are randomly intermixed in practice. However, subsequent skill retention is better for a randomly practiced group, an effect known as contextual interference (CI). The present study examined the neural substrates of CI using functional magnetic resonance imaging (fMRI). Individuals learned a set of three 4-element sequences with the left hand according to a block or random practice schedule. Behavioral retest for skill retention confirmed the presence of a typical CI effect with the random group outperforming the block group. Using a go/no-go fMRI paradigm, sequence preparation during the premovement study period was separated from movement execution. Imaging data for the two groups were compared for the first 1/3 and final 1/3 of training trials. Toward the end of training, behavioral performance between the two groups was similar, although the random group would later display a performance advantage on retention testing. During study time, the random group showed greater activity in sensorimotor and premotor regions compared to the block group. These areas are associated with motor preparation, sequencing, and response selection. This pattern of recruitment is consistent with the hypothesis that CI benefits in a sequencing task are due to improved capacity to actively prepare motor responses.

The Impact of Aesthetic Evaluation and Physical Ability on Dance Perception

The field of neuroaesthetics attracts attention from neuroscientists and artists interested in the neural underpinnings of esthetic experience. Though less studied than the neuroaesthetics of visual art, dance neuroaesthetics is a particularly rich subfield to explore, as it is informed not only by research on the neurobiology of aesthetics, but also by an extensive literature on how action experience shapes perception. Moreover, it is ideally suited to explore the embodied simulation account of esthetic experience, which posits that activation within sensorimotor areas of the brain, known as the action observation network (AON), is a critical element of the esthetic response. In the present study, we address how observers’ esthetic evaluation of dance is related to their perceived physical ability to reproduce the movements they watch. Participants underwent functional magnetic resonance imaging while evaluating how much they liked and how well they thought they could physically replicate a range of dance movements performed by professional ballet dancers. We used parametric analyses to evaluate brain regions that tracked with degree of liking and perceived physical ability. The findings reveal strongest activation of occipitotemporal and parietal portions of the AON when participants view movements they rate as both esthetically pleasing and difficult to reproduce. As such, these findings begin to illuminate how the embodied simulation account of esthetic experience might apply to watching dance, and provide preliminary evidence as to why some people find enjoyment in an evening at the ballet.

On-line grasp control is mediated by the contralateral hemisphere

Electrophysiological recordings from monkeys, as well as functional imaging and neuropsychological work with humans, have suggested that a region in the anterior portion of the intraparietal sulcus (aIPS) is involved in prehensile movements. With recent methodological advances using transcranial magnetic stimulation (TMS), we can now causally attribute anatomy with function to more precisely determine the specific involvement of aIPS in grasping. It has recently been demonstrated that aIPS is specifically involved in executing a grasp under conditions of both constant target requirements, as well as in correcting a movement under conditions in which a target perturbation occurs. In the present study, we extend these findings by determining the differential contribution of the left and right hemisphere to executing a grasping movement with the left and right hands. Transient disruption of left aIPS at movement onset impairs grasping with the right but not the left hand, and disruption of right aIPS impairs grasping with the left but not the right hand. We conclude that grasping is a lateralized process, relying exclusively on the contralateral hemisphere, and discuss the implications of these findings in relationship to models of hemispheric dominance for motor control.

Action observation in the infant brain: The role of body form and motion

Much research has been carried out to understand how human brains make sense of another agent in motion. Current views based on human adult and monkey studies assume a matching process in the motor system biased toward actions performed by conspecifics and present in the observers motor repertoire. However, little is known about the neural correlates of action cognition in early ontogeny. In this study, we examined the processes involved in the observation of full body movements in 4-month-old infants using functional near-infrared spectroscopy to measure localized brain activation. In a 2 × 2 design, infants watched human or robotic figures moving in a smooth, familiar human-like manner, or in a rigid, unfamiliar robot-like manner. We found that infant premotor cortex responded more strongly to observe robot-like motion compared with human-like motion. Contrary to current views, this suggests that the infant motor system is flexibly engaged by novel movement patterns. Moreover, temporal cortex responses indicate that infants integrate information about form and motion during action observation. The response patterns obtained in premotor and temporal cortices during action observation in these young infants are very similar to those reported for adults. These findings thus suggest that the brain processes involved in the analysis of an agent in motion in adults become functionally specialized very early in human development.

Representing others' actions: The role of expertise in the aging mind

A large body of evidence suggests that action execution and action observation share a common representational domain. To date, little is known about age-related changes in these action representations that are assumed to support various abilities such as the prediction of observed actions. The purpose of the present study was to investigate (a) how age affects the ability to predict the time course of observed actions; and (b) whether and to what extent sensorimotor expertise attenuates age-related declines in prediction performance. In a first experiment, older adults predicted the time course of familiar everyday actions less precisely than younger adults. In a second experiment, younger and older figure skating experts as well as age-matched novices were asked to predict the time course of figure skating elements and simple movement exercises. Both young age and sensorimotor expertise had a positive influence on prediction performance of figure skating elements. The expertise-related benefit did not show a transfer to movement exercises. Together, the results suggest a specific decline of action representations in the aging mind. However, extensive sensorimotor experience seems to enable experts to represent actions from their domain of expertise more precisely even in older age.

Contorted and ordinary body postures in the human brain

Social interaction and comprehension of non-verbal behaviour requires a representation of people’s bodies. Research into the neural underpinnings of body representation implicates several brain regions including extrastriate and fusiform body areas (EBA and FBA), superior temporal sulcus (STS), inferior frontal gyrus (IFG) and inferior parietal lobule (IPL). The different roles played by these regions in parsing familiar and unfamiliar body postures remain unclear. We examined the responses of this body observation network to static images of ordinary and contorted postures by using a repetition suppression design in functional neuroimaging. Participants were scanned whilst observing static images of a contortionist or a group of objects in either ordinary or unusual configurations, presented from different viewpoints. Greater activity emerged in EBA and FBA when participants viewed contorted compared to ordinary body postures. Repeated presentation of the same posture from different viewpoints lead to suppressed responses in the fusiform gyrus as well as three regions that are characteristically activated by observing moving bodies, namely STS, IFG and IPL. These four regions did not distinguish the image viewpoint or the plausibility of the posture. Together, these data define a broad cortical network for processing static body postures, including regions classically associated with action observation.

Action Prediction in Younger versus Older Adults: Neural Correlates of Motor Familiarity

Generating predictions during action observation is essential for efficient navigation through our social environment. With age, the sensitivity in action prediction declines. In younger adults, the action observation network (AON), consisting of premotor, parietal and occipitotemporal cortices, has been implicated in transforming executed and observed actions into a common code. Much less is known about age-related changes in the neural representation of observed actions. Using fMRI, the present study measured brain activity in younger and older adults during the prediction of temporarily occluded actions (figure skating elements and simple movement exercises). All participants were highly familiar with the movement exercises whereas only some participants were experienced figure skaters. With respect to the AON, the results confirm that this network was preferentially engaged for the more familiar movement exercises. Compared to younger adults, older adults recruited visual regions to perform the task and, additionally, the hippocampus and caudate when the observed actions were familiar to them. Thus, instead of effectively exploiting the sensorimotor matching properties of the AON, older adults seemed to rely predominantly on the visual dynamics of the observed actions to perform the task. Our data further suggest that the caudate played an important role during the prediction of the less familiar figure skating elements in better-performing groups. Together, these findings show that action prediction engages a distributed network in the brain, which is modulated by the content of the observed actions and the age and experience of the observer.

The control of automatic imitation based on bottom—up and top—down cues to animacy: Insights from brain and behavior

Humans automatically imitate other peoples actions during social interactions, building rapport and social closeness in the process. Although the behavioral consequences and neural correlates of imitation have been studied extensively, little is known about the neural mechanisms that control imitative tendencies. For example, the degree to which an agent is perceived as human-like influences automatic imitation, but it is not known how perception of animacy influences brain circuits that control imitation. In the current fMRI study, we examined how the perception and belief of animacy influence the control of automatic imitation. Using an imitation–inhibition paradigm that involves suppressing the tendency to imitate an observed action, we manipulated both bottom–up (visual input) and top–down (belief) cues to animacy. Results show divergent patterns of behavioral and neural responses. Behavioral analyses show that automatic imitation is equivalent when one or both cues to animacy are present but reduces when both are absent. By contrast, right TPJ showed sensitivity to the presence of both animacy cues. Thus, we demonstrate that right TPJ is biologically tuned to control imitative tendencies when the observed agent both looks like and is believed to be human. The results suggest that right TPJ may be involved in a specialized capacity to control automatic imitation of human agents, rather than a universal process of conflict management, which would be more consistent with generalist theories of imitative control. Evidence for specialized neural circuitry that “controls” imitation offers new insight into developmental disorders that involve atypical processing of social information, such as autism spectrum disorders.