Priming of hand and foot response: is spatial attention to the body site enough?

The purpose of the present study was to test whether we see evidence for body compatibility effects when viewing both familiar and unusual body postures. Specifically, in a task where colour targets have to be discriminated, we tested whether spatial orienting to a body site is sufficient for effects of body compatibility to emerge when viewing a task-irrelevant body or whether effects are dependent on whether or not we are able to adopt the viewed body posture. The results suggest that spatial orienting to a body site is insufficient; rather we argue that it is only postures that are familiar and we are easily able to adopt that can be processed fluently and influence target discrimination. This points to a key contribution of motor representations to body compatibility effects.

Testing key predictions of the associative account of mirror neurons in humans using multivariate pattern analysis.

Cook et al. overstate the evidence supporting their associative account of mirror neurons in humans: most studies do not address a key property, action-specificity that generalizes across the visual and motor domains. Multivariate pattern analysis (MVPA) of neuroimaging data can address this concern, and we illustrate how MVPA can be used to test key predictions of their account.

Facilitation and interference in spatial and body reference frames.

The observation of someone else's action facilitates similar actions in the observer. Such priming effects can be driven by alignment between the observer and the observed in body-centred or spatial coordinates (or both). The separate and joint contributions of these sources of priming remain to be fully characterised. Here, we compare spatial and body priming effects across the whole body "space", by using hand and foot responses. This allows a clearer separation of body priming from spatial priming than available from previous studies. In addition, we demonstrate two further features of these action priming effects. First, there are general interference and facilitation effects when the layout of viewed displays matches the participant's body (e.g. hand above the foot). These effects have not been considered in previous studies. Second, by taking these layout effects into account, we identify the facilitation and interference components of spatial and body priming effects. Both types of priming effect are observed, and facilitation and interference effects are only observed when both body and spatial frames of reference are working in the same direction. These findings show that in action perception, the behaviours of others are processed simultaneously in multiple frames of reference that have complex, interacting effects--both facilitating and interfering--on the motor system of the observer.

Doing, seeing, or both: effects of learning condition on subsequent action perception.

It has been proposed that common codes for vision and action emerge from associations between an individual's production and simultaneous observation of actions. This typically first-person view of one's own action subsequently transfers to the third-person view when observing another individual. We tested vision-action associations and the transfer from first-person to third-person perspective by comparing novel hand-action sequences that were learned under three conditions: first, by being performed and simultaneously viewed from a first-person perspective; second, by being performed but not seen; and third, by being seen from a first-person view without being executed. We then used functional magnetic resonance imaging (fMRI) to compare the response to these three types of learned action sequences when they were presented from a third-person perspective. Visuomotor areas responded most strongly to sequences that were learned by simultaneously producing and observing the action sequences. We also note an important asymmetry between vision and action: Action sequences learned by performance alone, in the absence of vision, facilitated the emergence of visuomotor responses, whereas action sequences learned by viewing alone had comparably little effect. This dominance of action over vision supports the notion of forward/predictive models of visuomotor systems.

Learning associations between action and perception: effects of incompatible training on body part and spatial priming.

Observation of another person executing an action primes the same action in the observer's motor system. Recent evidence has shown that these priming effects are flexible, where training of new associations, such as making a foot response when viewing a moving hand, can reduce standard action priming effects (Gillmeister, Catmur, Liepelt, Brass, & Heyes, 2008). Previously, these effects were obtained after explicit learning tasks in which the trained action was cued by the content of a visual stimulus. Here we report similar learning processes in an implicit task in which the participant's action is self-selected, and subsequent visual effects are determined by the nature of that action. Importantly, we show that these learning processes are specific to associations between actions and viewed body parts, in that incompatible spatial training did not influence body part or spatial priming effects. Our results are consistent with models of visuomotor learning that place particular emphasis on the repeated experience of watching oneself perform an action.

Representation of action in occipito-temporal cortex.

A fundamental question for social cognitive neuroscience is how and where in the brain the identities and actions of others are represented. Here we present a replication and extension of a study by Kable and Chatterjee [Kable, J. W., & Chatterjee, A. Specificity of action representations in the lateral occipito-temporal cortex. Journal of Cognitive Neuroscience, 18, 1498-1517, 2006] examining the role of occipito-temporal cortex in these processes. We presented full-cue movies of actors performing whole-body actions and used fMRI to test for action- and identity-specific adaptation effects. We examined a series of functionally defined regions, including the extrastriate and fusiform body areas, the fusiform face area, the parahippocampal place area, the lateral occipital complex, the right posterior superior temporal sulcus, and motion-selective area hMT+. These regions were analyzed with both standard univariate measures as well as multivoxel pattern analyses. Additionally, we performed whole-brain tests for significant adaptation effects. We found significant action-specific adaptation in many areas, but no evidence for identity-specific adaptation. We argue that this finding could be explained by differences in the familiarity of the stimuli presented: The actions shown were familiar but the actors performing the actions were unfamiliar. However, in contrast to previous findings, we found that the action adaptation effect could not be conclusively tied to specific functionally defined regions. Instead, our results suggest that the adaptation to previously seen actions across identities is a widespread effect, evident across lateral and ventral occipito-temporal cortex.

Surface-based information mapping reveals crossmodal vision-action representations in human parietal and occipitotemporal cortex.

Many lines of evidence point to a tight linkage between the perceptual and motoric representations of actions. Numerous demonstrations show how the visual perception of an action engages compatible activity in the observer's motor system. This is seen for both intransitive actions (e.g., in the case of unconscious postural imitation) and transitive actions (e.g., grasping an object). Although the discovery of "mirror neurons" in macaques has inspired explanations of these processes in human action behaviors, the evidence for areas in the human brain that similarly form a crossmodal visual/motor representation of actions remains incomplete. To address this, in the present study, participants performed and observed hand actions while being scanned with functional MRI. We took a data-driven approach by applying whole-brain information mapping using a multivoxel pattern analysis (MVPA) classifier, performed on reconstructed representations of the cortical surface. The aim was to identify regions in which local voxelwise patterns of activity can distinguish among different actions, across the visual and motor domains. Experiment 1 tested intransitive, meaningless hand movements, whereas experiment 2 tested object-directed actions (all right-handed). Our analyses of both experiments revealed crossmodal action regions in the lateral occipitotemporal cortex (bilaterally) and in the left postcentral gyrus/anterior parietal cortex. Furthermore, in experiment 2 we identified a gradient of bias in the patterns of information in the left hemisphere postcentral/parietal region. The postcentral gyrus carried more information about the effectors used to carry out the action (fingers vs. whole hand), whereas anterior parietal regions carried more information about the goal of the action (lift vs. punch). Taken together, these results provide evidence for common neural coding in these areas of the visual and motor aspects of actions, and demonstrate further how MVPA can contribute to our understanding of the nature of distributed neural representations.

fMRI-adaptation studies of viewpoint tuning in the extrastriate and fusiform body areas.

People are easily able to perceive the human body across different viewpoints, but the neural mechanisms underpinning this ability are currently unclear. In three experiments, we used functional MRI (fMRI) adaptation to study the view-invariance of representations in two cortical regions that have previously been shown to be sensitive to visual depictions of the human body--the extrastriate and fusiform body areas (EBA and FBA). The BOLD response to sequentially presented pairs of bodies was treated as an index of view invariance. Specifically, we compared trials in which the bodies in each image held identical poses (seen from different views) to trials containing different poses. EBA and FBA adapted to identical views of the same pose, and both showed a progressive rebound from adaptation as a function of the angular difference between views, up to approximately 30 degrees. However, these adaptation effects were eliminated when the body stimuli were followed by a pattern mask. Delaying the mask onset increased the response (but not the adaptation effect) in EBA, leaving FBA unaffected. We interpret these masking effects as evidence that view-dependent fMRI adaptation is driven by later waves of neuronal responses in the regions of interest. Finally, in a whole brain analysis, we identified an anterior region of the left inferior temporal sulcus (l-aITS) that responded linearly to stimulus rotation, but showed no selectivity for bodies. Our results show that body-selective cortical areas exhibit a similar degree of view-invariance as other object selective areas--such as the lateral occipitotemporal area (LO) and posterior fusiform gyrus (pFs).

Dissociation of extrastriate body and biological-motion selective areas by manipulation of visual-motor congruency.

To date, several posterior brain regions have been identified that play a role in the visual perception of other people and their movements. The aim of the present study is to understand how these areas may be involved in relating body movements to their visual consequences. We used fMRI to examine the extrastriate body area (EBA), the fusiform body area (FBA), and an area in the posterior superior temporal sulcus (pSTS) that responds to patterns of human biological motion. Each area was localized in individual participants with independent scans. In the main experiment, participants performed and/or viewed simple, intransitive hand actions while in the scanner. An MR-compatible camera with a near-egocentric view of the participant's hand was used to manipulate the relationship between motor output and the visual stimulus. Participants' only view of their hands was via this camera. In the Compatible condition, participants viewed their own live hand movements projected onto the screen. In the Incompatible condition, participants viewed actions that were different from the actions they were executing. In pSTS, the BOLD response in the Incompatible condition was significantly higher than in the Compatible condition. Further, the response in the Compatible condition was below baseline, and no greater than that found in a control condition in which hand actions were performed without any visual input. This indicates a strong suppression in pSTS of the response to the visual stimulus that arises from one's own actions. In contrast, in EBA and FBA, we found a large but equivalent response to the Compatible and Incompatible conditions, and this response was the same as that elicited in a control condition in which hand actions were viewed passively, with no concurrent motor task. These findings indicate that, in contrast to pSTS, EBA and FBA are decoupled from motor systems. Instead we propose that their role is limited to perceptual analysis of body-related visual input.

Animate and inanimate objects in human visual cortex: Evidence for task-independent category effects.

Evidence from neuropsychology suggests that the distinction between animate and inanimate kinds is fundamental to human cognition. Previous neuroimaging studies have reported that viewing animate objects activates ventrolateral visual brain regions, whereas inanimate objects activate ventromedial regions. However, these studies have typically compared only a small number of animate and inanimate kinds (e.g. animals and tools) and some evidence indicates that task demands determine whether these effects occur at all. In the current study we test whether a lateral-medial animacy bias is evident across a variety of stimuli, and across different tasks (matching two stimuli at a general, intermediate and exemplar level). Images of objects were presented sequentially in pairs, and match/mismatch judgements were made at different levels in different scans. The fMRI data showed ventrolateral activation for animate objects and ventromedial activation for inanimate objects. Additional analyses within these regions revealed no main effect of task, and no interactions between task and animacy. Furthermore, there were no subpopulations of voxels in any of the regions of interest that showed a significant task by animacy interaction. We conclude that ventral animate/inanimate category biases do not always depend on top-down task orientation. Furthermore, we consider whether the animate and inanimate activations reflect biases in the non-preferred responses of strongly category-selective regions such as the fusiform face area or the parahippocampal place area.

The face network: overextended? (Comment on: "Let's face it: It's a cortical network" by Alumit Ishai).

We offer a critique of Ishai's [Ishai, A., 2008. Let's face it: it's a cortical network. NeuroImage. doi:10.1016/j.neuroimage.2007.10.040] comment on the value of considering the brain areas that support face perception as a network. We emphasise that this idea is not in opposition to the notion that the fusiform gyrus plays a key role in the visual analysis of faces. More important, we argue that the definition offered of the "extended" face network--areas showing a greater fMRI response to intact than scrambled face images--is too inclusive, and present data to indicate that at least two of the proposed "nodes" of this network also respond to non-face objects (compared to scrambled controls). Finally, we consider briefly how converging methodological approaches may augment the use of fMRI alone in understanding how anatomically widespread brain areas coordinate their activity in order to make sense of the human face.

Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas.

This study examined the contributions of two previously identified brain regions-the extrastriate and fusiform body areas (EBA and FBA)-to the visual representation of the human form. Specifically we measured in these two areas the magnitude of fMRI response as a function of the amount of the human figure that is visible in the image, in the range from a single finger to the entire body. A second experiment determined the selectivity of these regions for body and body part stimuli relative to closely matched control images. We found a gradual increase in the selectivity of the EBA as a function of the amount of body shown. In contrast, the FBA shows a steplike function, with no significant selectivity for individual fingers or hands. In a third experiment we demonstrate that the response pattern seen in EBA does not extend to adjacent motion-selective human midtemporal area. We propose an interpretation of these results by analogy to nearby face-selective regions occipital face area (OFA) and fusiform face area (FFA). Specifically, we hypothesize that the EBA analyzes bodies at the level of parts (as has been proposed for faces in the OFA), whereas FBA (by analogy to FFA) may have a role in processing the configuration of body parts into wholes.

Functional magnetic resonance imaging investigation of overlapping lateral occipitotemporal activations using multi-voxel pattern analysis.

Several functional areas are proposed to reside in human lateral occipitotemporal cortex, including the motion-selective human homolog of macaque area MT (hMT), object-form-selective lateral occipital complex (LO), and body-selective extrastriate body area (EBA). Indeed, several functional magnetic resonance imaging (fMRI) studies have reported significant activation overlap among these regions. The standard interpretation of this overlap would be that the common areas of activation reflect engagement of common neural systems. Alternatively, motion, object form, and body form may be processed independently within this general region. To distinguish these possibilities, we first analyzed the lateral occipitotemporal responses to motion, objects, bodies, and body parts with whole-brain group-average analyses and within-subjects functional region of interest (ROI) analyses. The activations elicited by these stimuli, each relative to a matched control, overlapped substantially in the group analysis. When hMT, LO, and EBA were defined functionally within subjects, each ROI in each hemisphere (except right-hemisphere hMT) showed significant selectivity for motion, intact objects, bodies, and body parts, although only the peak voxel of each region was tested. In contrast, multi-voxel analyses of variations in selectivity patterns revealed that visual motion, object form, and the form of the human body elicited three relatively independent patterns of fMRI activity in lateral occipitotemporal cortex. Multi-voxel approaches, in contrast to other methods, can reveal the functional significance of overlapping fMRI activity in extrastriate cortex and, by extension, elsewhere in the brain.

Patterns of fMRI activity dissociate overlapping functional brain areas that respond to biological motion.

Accurate perception of the actions and intentions of other people is essential for successful interactions in a social environment. Several cortical areas that support this process respond selectively in fMRI to static and dynamic displays of human bodies and faces. Here we apply pattern-analysis techniques to arrive at a new understanding of the neural response to biological motion. Functionally defined body-, face-, and motion-selective visual areas all responded significantly to "point-light" human motion. Strikingly, however, only body selectivity was correlated, on a voxel-by-voxel basis, with biological motion selectivity. We conclude that (1) biological motion, through the process of structure-from-motion, engages areas involved in the analysis of the static human form; (2) body-selective regions in posterior fusiform gyrus and posterior inferior temporal sulcus overlap with, but are distinct from, face- and motion-selective regions; (3) the interpretation of region-of-interest findings may be substantially altered when multiple patterns of selectivity are considered.

The role of the extrastriate body area in action perception.

Numerous cortical regions respond to aspects of the human form and its actions. What is the contribution of the extrastriate body area (EBA) to this network? In particular, is the EBA involved in constructing a dynamic representation of observed actions? We scanned 16 participants with fMRI while they viewed two kinds of stimulus sequences. In the coherent condition, static frames from a movie of a single, intransitive whole-body action were presented in the correct order. In the incoherent condition, a series of frames from multiple actions (involving one actor) were presented. ROI analyses showed that the EBA, unlike area MT + and the posterior superior temporal sulcus, responded more to the incoherent than to the coherent conditions. Whole brain analyses revealed increased activation to the coherent sequences in parietal and frontal regions that have been implicated in the observation and control of movement. We suggest that the EBA response adapts when succeeding images depict relatively similar postures (coherent condition) compared to relatively different postures (incoherent condition). We propose that the EBA plays a unique role in the perception of action, by representing the static structure, rather than dynamic aspects, of the human form.