Jan Jastorff

Coding Observed Motor Acts: Different Organizational Principles in the Parietal and Premotor Cortex of Humans

Understanding actions of conspecifics is a fundamental social ability depending largely on the activation of a parieto-frontal network. Using functional MRI (fMRI), we studied how goal-directed movements (i.e., motor acts) performed by others are coded within this network. In the first experiment, we presented volunteers with video clips showing four different motor acts (dragging, dropping, grasping, and pushing) performed with different effectors (foot, hand, and mouth). We found that the coding of observed motor acts differed between premotor and parietal cortex. In the premotor cortex, they clustered according to the effector used, and in the inferior parietal lobule (IPL), they clustered according to the type of the observed motor act, regardless of the effector. Two subsequent experiments in which we directly contrasted these four motor acts indicated that, in IPL, the observed motor acts are coded according to the relationship between agent and object: Movements bringing the object toward the agent (grasping and dragging) activate a site corresponding approximately to the ventral part of the putative human AIP (phAIP), whereas movements moving the object away from the agent (pushing and dropping) are clustered dorsally within this area. These data provide indications that the phAIP region plays a role in categorizing motor acts according to their behavioral significance. In addition, our results suggest that in the case of motor acts typically done with the hand, the representations of such acts in phAIP are used as templates for coding motor acts executed with other effectors.

Integration of shape and motion cues in biological motion processing in the monkey STS.

To correctly perceive biological actions, the movement pattern generated in the course of the action has to be linked to the configuration of the actor. Recently, we showed that in humans, motion and configuration cues are processed separately in occipito-temporal cortex, and that both cues are integrated in the extrastriate (EBA) and fusiform (FBA) body areas (Jastorff and Orban, 2009). Using the same factorial design as in our human study, we performed fMRI experiments in awake monkeys to compare biological motion processing in the two species. Point-light displays of monkeys engaged in various actions were presented in a 2×2 factorial design. One factor manipulated the configuration of the stimuli, the other, the kinematics. As in humans, the two factors were anatomically segregated in the superior temporal sulcus (STS) rostral to the MT/V5 complex, with the effect of configuration significant along the lower bank and that of kinematics significant in the fundus and the upper bank of the STS. Moreover, voxels showing a significant interaction between the two factors were mainly confined to body-selective patches within the STS, mimicking our human findings. Importantly, this study reports for the first time differential activation for biological actions presented as point-light displays in the monkey. Moreover, our results suggest that the processing mechanisms of biological actions are remarkably similar in humans and macaque monkeys, and provide the basis for linking existing and future single-cell physiology in the monkey with human functional imaging.

The overlap of the EBA and the MT/V5 cluster

The extrastriate body area (EBA) is located in the lateral occipito-temporal cortex, in the vicinity of the motion-sensitive region hMT/V5+. To investigate the relationship of EBA to the recently mapped retinotopic areas of the MT/V5 cluster (Kolster et al., 2010), we evaluated the proportion of voxels responsive to the presentation of static human bodies (EBA voxels) in each of the four areas of the MT/V5 cluster and neighboring LO and phPIT areas. We evaluated this proportion as both a function of the number of voxels in a given area and the total number of voxels in a broader lateral occipito-temporal cortex (LOTC) ROI. We observed that each of the four retinotopic areas of the MT/V5 cluster includes substantial fractions of EBA voxels, in contrast to the LO and phPIT areas. This proportion was slightly greater in the right than left hemisphere, and did not depend on the control condition. While most EBA voxels in MT/V5 were only body-sensitive, those in pMSTv and pFST were also motion-sensitive. The main locus of EBA voxels outside the MT/V5 cluster was in the LOTC cortex just rostral to the MT/V5 cluster. Although this region contained more EBA voxels than the MT/V5 cluster, the proportion as a function of areal size was much reduced compared to the MT/V5 cluster. Our results show that EBA is not a single cortical area as EBA voxels are located in all four areas of the MT/V5 cluster, and that body-sensitivity is a key feature of the MT/V5 cluster, in keeping with its exquisite sensitivity to observed actions of others.

Common and Segregated Processing of Observed Actions in Human SPL

To clarify the functional organization of parietal cortex involved in action observation, we scanned subjects observing 3 widely different classes of actions: Manipulation with the hands, locomotion, and climbing. An effector-based organization predicts that parietal regions involved in the observation of climbing should not differ from those involved in observing manipulation and locomotion, opposite to the prediction of an organization based upon the action performed. Compared with individual controls, the observation of climbing evoked activity in dorsal superior parietal lobule (SPL), extending into precuneus and posterior cingulate sulcus. Observation of locomotion differentially activated similar regions less strongly. Observation of manipulation activated ventro-rostral SPL, including putative human AIP (phAIP). Using interaction testing and exclusive masking to directly compare the parietal regions involved in observing the 3 action classes, relative to the controls, revealed that the rostral part of dorsal SPL was specifically involved in observing climbing and phAIP in observing manipulation. Parietal regions common to observing all 3 action classes were restricted and likely reflected higher order visual processing of body posture and 3D structure from motion. These results support a functional organization of some parietal regions involved in action observation according to the type of action in the case of climbing and manipulation.

Fine-grained stimulus representations in body selective areas of human occipito-temporal cortex.

Neurophysiological and functional imaging studies have investigated the representation of animate and inanimate stimulus classes in monkey inferior temporal (IT) and human occipito-temporal cortex (OTC). These studies proposed a distributed representation of stimulus categories across IT and OTC and at the same time highlighted category specific modules for the processing of bodies, faces and objects. Here, we investigated whether the stimulus representation within the extrastriate (EBA) and the fusiform (FBA) body areas differed from the representation across OTC. To address this question, we performed an event-related fMRI experiment, evaluating the pattern of activation elicited by 200 individual stimuli that had already been extensively tested in our earlier monkey imaging and single cell studies (Popivanov et al., 2012, 2014). The set contained achromatic images of headless monkey and human bodies, two sets of man-made objects, monkey and human faces, four-legged mammals, birds, fruits, and sculptures. The fMRI response patterns within EBA and FBA primarily distinguished bodies from non-body stimuli, with subtle differences between the areas. However, despite responding on average stronger to bodies than to other categories, classification performance for preferred and non-preferred categories was comparable. OTC primarily distinguished animate from inanimate stimuli. However, cluster analysis revealed a much more fine-grained representation with several homogeneous clusters consisting entirely of stimuli of individual categories. Overall, our data suggest that category representation varies with location within OTC. Nevertheless, body modules contain information to discriminate also non-preferred stimuli and show an increasing specificity in a posterior to anterior gradient.

Cortical regions involved in the observation of bimanual actions

Although we are beginning to understand how observed actions performed by conspecifics with a single hand are processed and how bimanual actions are controlled by the motor system, we know very little about the processing of observed bimanual actions. We used fMRI to compare the observation of bimanual manipulative actions with their unimanual components, relative to visual control conditions equalized for visual motion. Bimanual action observation did not activate any region specialized for processing visual signals related to this more elaborated action. On the contrary, observation of bimanual and unimanual actions activated similar occipito-temporal, parietal and premotor networks. However, whole-brain as well as region of interest (ROI) analyses revealed that this network functions differently under bimanual and unimanual conditions. Indeed, in bimanual conditions, activity in the network was overall more bilateral, especially in parietal cortex. In addition, ROI analyses indicated bilateral parietal activation patterns across hand conditions distinctly different from those at other levels of the action-observation network. These activation patterns suggest that while occipito-temporal and premotor levels are involved with processing the kinematics of the observed actions, the parietal cortex is more involved in the processing of static, postural aspects of the observed action. This study adds bimanual cooperation to the growing list of distinctions between parietal and premotor cortex regarding factors affecting visual processing of observed actions.

Amygdala atrophy affects emotion-related activity in face-responsive regions in frontotemporal degeneration

In the healthy brain, modulatory influences from the amygdala commonly explain enhanced activation in face-responsive areas by emotional facial expressions relative to neutral expressions. In the behavioral variant frontotemporal dementia (bvFTD) facial emotion recognition is impaired and has been associated with atrophy of the amygdala. By combining structural and functional MRI in 19 patients with bvFTD and 20 controls we investigated the neural effects of emotion in face-responsive cortex and its relationship with amygdalar gray matter (GM) volume in neurodegeneration. Voxel-based morphometry revealed decreased GM volume in anterior medio-temporal regions including amygdala in patients compared to controls. During fMRI, we presented dynamic facial expressions (fear and chewing) and their spatiotemporally scrambled versions. We found enhanced activation for fearful compared to neutral faces in ventral temporal cortex and superior temporal sulcus in controls, but not in patients. In the bvFTD group left amygdalar GM volume correlated positively with emotion-related activity in left fusiform face area (FFA). This correlation was amygdala-specific and driven by GM in superficial and basolateral (BLA) subnuclei, consistent with reported amygdalar-cortical networks. The data suggests that anterior medio-temporal atrophy in bvFTD affects emotion processing in distant posterior areas.

Acting Alters Visual Processing: Flexible Recruitment of Visual Areas by One's Own Actions

Using functional magnetic resonance imaging, we investigated the effect of motor preparation/execution on the activation of visual cortical areas by action observation. We presented videos of human actors performing several fine manipulative actions (e.g., grasping) with the hand or foot, together with appropriate control stimuli. Subjects either responded in a central fixation task with the hand (A) or foot (B) or viewed the stimuli passively (C). Experimental conditions were arranged according to a 2 × 2 × 3 factorial design with action, effector, and response as factors. Bilateral posterior parietal cortex was more strongly activated for action videos compared with controls during active runs (A or B) contrasted with passive runs (C). Two neighboring regions in the right fusiform gyrus (FG) were activated when the effector employed to respond in the task matched that displayed in the videos (A or B), independently of whether the stimulus was an action or a control. Neighboring regions in the right posterior middle temporal gyrus (MTG) were also activated when the effector observed and that used to respond matched (A or B), but only for action videos, not controls. Our results indicate flexible modulation of visual areas during concurrent action observation and action execution/preparation, which was effector specific in the FG and MTG.

Functional dissociation between anterior temporal lobe and inferior frontal gyrus in the processing of dynamic body expressions: Insights from behavioral variant frontotemporal dementia.

Several brain regions are involved in the processing of emotional stimuli, however, the contribution of specific regions to emotion perception is still under debate. To investigate this issue, we combined behavioral testing, structural and resting state imaging in patients diagnosed with behavioral variant frontotemporal dementia (bvFTD) and age matched controls, with task‐based functional imaging in young, healthy volunteers. As expected, bvFTD patients were impaired in emotion detection as well as emotion categorization tasks, testing dynamic emotional body expressions as stimuli. Interestingly, their performance in the two tasks correlated with gray matter volume in two distinct brain regions, the left anterior temporal lobe for emotion detection and the left inferior frontal gyrus (IFG) for emotion categorization. Confirming this observation, multivoxel pattern analysis in healthy volunteers demonstrated that both ROIs contained information for emotion detection, but that emotion categorization was only possible from the pattern in the IFG. Furthermore, functional connectivity analysis showed reduced connectivity between the two regions in bvFTD patients. Our results illustrate that the mentalizing network and the action observation network perform distinct tasks during emotion processing. In bvFTD, communication between the networks is reduced, indicating one possible cause underlying the behavioral symptoms. Hum Brain Mapp 37:4472–4486, 2016.

Common neural correlates of emotion perception in humans

Whether neuroimaging findings support discriminable neural correlates of emotion categories is a longstanding controversy. Two recent meta‐analyses arrived at opposite conclusions, with one supporting (Vytal and Hamann [ ]: J Cogn Neurosci 22:2864–2885) and the other opposing this proposition (Lindquist et al. [ ]: Behav Brain Sci 35:121–143). To obtain direct evidence regarding this issue, we compared activations for four emotions within a single fMRI design. Angry, happy, fearful, sad and neutral stimuli were presented as dynamic body expressions. In addition, observers categorized motion morphs between neutral and emotional stimuli in a behavioral experiment to determine their relative sensitivities. Brain–behavior correlations revealed a large brain network that was identical for all four tested emotions. This network consisted predominantly of regions located within the default mode network and the salience network. Despite showing brain–behavior correlations for all emotions, muli‐voxel pattern analyses indicated that several nodes of this emotion general network contained information capable of discriminating between individual emotions. However, significant discrimination was not limited to the emotional network, but was also observed in several regions within the action observation network. Taken together, our results favor the position that one common emotional brain network supports the visual processing and discrimination of emotional stimuli. Hum Brain Mapp 36:4184–4201, 2015.