Lennart Verhagen

The rubber hand illusion in action

In the well-known rubber hand illusion (RHI), watching a rubber hand being stroked while ones own unseen hand is synchronously stroked, induces a relocation of the sensed position of ones own hand towards the rubber hand [Botvinick, M., & Cohen, J. (1998). Rubber hands feel touch that eyes see. Nature, 391(6669), 756]. As one has lost the veridical location of ones hand, one should not be able to correctly guide ones hand movements. An accurate representation of the location of body parts is indeed a necessary pre-requisite for any correct motor command [Graziano, M. S. A., & Botvinick, M. M. (1999). How the brain represents the body: Insights from neurophysiology and psychology. In D. Gopher, & A. Koriat (Eds.), Attention and performance XVII-Cognitive regulation of performance interaction of theory and application (pp. 136-157)]. However, it has not yet been investigated whether action is indeed affected by the proprioceptive drift towards the rubber hand, nor has the resistance of visual capture in the RHI to new proprioceptive information been assessed. In the present two kinematic experiments, we show for the first time that action resists the RHI and that the RHI resists action. In other words, we show a dissociation between illusion-insensitive ballistic motor responses and illusion-sensitive perceptual bodily judgments. Moreover, the stimulated hand was judged closer to the rubber hand for the perceptual responses, even after active movements. This challenges the view that any proprioceptive update through active movement of the stimulated hand erases the illusion. These results expand the knowledge about representations of the body in the healthy brain, and are in line with the currently most used dissociation between two types of body representations so far mainly based on neuropsychological patients [Paillard, J. (1991). Knowing where and knowing how to get there. In J. Paillard (Ed.), Brain and space (pp. 461-481); Paillard, J. (1999). Body schema and body image: A double dissociation in deafferented patients. In G. N. Gantchev, S. Mori, & J.Massion (Eds.), Motor control, today and tomorrow (pp. 197-214)].

Endogenous Testosterone Modulates Prefrontal–Amygdala Connectivity during Social Emotional Behavior

It is clear that the steroid hormone testosterone plays an important role in the regulation of social emotional behavior, but it remains unknown which neural circuits mediate these hormonal influences in humans. We investigated the modulatory effects of endogenous testosterone on the control of social emotional behavior by applying functional magnetic resonance imaging while healthy male participants performed a social approach–avoidance task. This task operationalized social emotional behavior by having participants approach and avoid emotional faces by pulling and pushing a joystick, respectively. Affect-congruent trials mapped the automatic tendency to approach happy faces and avoid angry faces. Affect-incongruent trials required participants to override those automatic action tendencies and select the opposite response (approach-angry, avoid-happy). The social emotional control required by affect-incongruent responses resulted in longer reaction times (RTs) and increased activity at the border of the ventrolateral prefrontal cortex and frontal pole (VLPFC/FP). We show that endogenous testosterone modulates these cerebral congruency effects through 2 mechanisms. First, participants with lower testosterone levels generate larger VLPFC/FP responses during affect-incongruent trials. Second, during the same trials, endogenous testosterone modulates the effective connectivity between the VLPFC/FP and the amygdala. These results indicate that endogenous testosterone influences local prefrontal activity and interregional connectivity supporting the control of social emotional behavior.

Is this hand for real? attenuation of the rubber hand illusion by transcranial magnetic stimulation over the inferior parietal lobule

In the rubber hand illusion (RHI), participants incorporate a rubber hand into a mental representation of ones body. This deceptive feeling of ownership is accompanied by recalibration of the perceived position of the participants real hand toward the rubber hand. Neuroimaging data suggest involvement of the posterior parietal lobule during induction of the RHI, when recalibration of the real hand toward the rubber hand takes place. Here, we used off-line low-frequency repetitive transcranial magnetic stimulation (rTMS) in a double-blind, sham-controlled within-subjects design to investigate the role of the inferior posterior parietal lobule (IPL) in establishing the RHI directly. Results showed that rTMS over the IPL attenuated the strength of the RHI for immediate perceptual body judgments only. In contrast, delayed perceptual responses were unaffected. Furthermore, ballistic action responses as well as subjective self-reports of feeling of ownership over the rubber hand remained unaffected by rTMS over the IPL. These findings are in line with previous research showing that the RHI can be broken down into dissociable bodily sensations. The illusion does not merely affect the embodiment of the rubber hand but also influences the experience and localization of ones own hand in an independent manner. Finally, the present findings concur with a multicomponent model of somatosensory body representations, wherein the IPL plays a pivotal role in subserving perceptual body judgments, but not actions or higher-order affective bodily judgments.

Perceptuo-Motor Interactions during Prehension Movements

Adaptive behavior relies on the integration of perceptual and motor processes. In this study, we aimed at characterizing the cerebral processes underlying perceptuo-motor interactions evoked during prehension movements in healthy humans, as measured by means of functional magnetic resonance imaging. We manipulated the viewing conditions (binocular or monocular) during planning of a prehension movement, while parametrically varying the slant of the grasped object. This design manipulates the relative relevance and availability of different depth cues necessary for accurate planning of the prehension movement, biasing visual information processing toward either the dorsal visual stream (binocular vision) or the ventral visual stream (monocular vision). Two critical nodes of the dorsomedial visuomotor stream [V6A (anterior visual area 6) and PMd (dorsal premotor cortex)] increased their activity with increasing object slant, regardless of viewing conditions. In contrast, areas in both the dorsolateral visuomotor stream [anterior intraparietal area (AIP) and ventral premotor cortex (PMv)] and in the ventral visual stream [lateral-occipital tactile-visual area (LOtv)] showed differential slant-related responses, with activity increasing when monocular viewing conditions and increasing slant required the processing of pictorial depth cues. These conditions also increased the functional coupling of AIP with both LOtv and PMv. These findings support the view that the dorsomedial stream is automatically involved in processing visuospatial parameters for grasping, regardless of viewing conditions or object characteristics. In contrast, the dorsolateral stream appears to adapt motor behavior to the current conditions by integrating perceptual information processed in the ventral stream into the prehension plan.

Anterior Prefrontal Cortex Inhibition Impairs Control over Social Emotional Actions

When dealing with emotional situations, we often need to rapidly override automatic stimulus-response mappings and select an alternative course of action [1], for instance, when trying to manage, rather than avoid, anothers aggressive behavior. The anterior prefrontal cortex (aPFC) has been linked to the control of these social emotional behaviors [2, 3]. We studied how this control is implemented by inhibiting the left aPFC with continuous theta burst stimulation (cTBS; [4]). The behavioral and cerebral consequences of this intervention were assessed with a task quantifying the control of social emotional actions and with concurrent measurements of brain perfusion. Inhibition of the aPFC led participants to commit more errors when they needed to select rule-driven responses overriding automatic action tendencies evoked by emotional faces. Concurrently, task-related perfusion decreased in bilateral aPFC and posterior parietal cortex and increased in amygdala and left fusiform face area. We infer that the aPFC controls social emotional behavior by upregulating regions involved in rule selection [5] and downregulating regions supporting the automatic evaluation of emotions [6]. These findings illustrate how exerting emotional control during social interactions requires the aPFC to coordinate rapid action selection processes, the detection of emotional conflicts, and the inhibition of emotionally-driven responses.

Cortical dynamics of sensorimotor integration during grasp planning

Our sensorimotor interactions with objects are guided by their current spatial and perceptual features, as well as by learned object knowledge. A fresh red tomato is grasped differently than a soft overripe tomato, even when those objects possess the same spatial metrics of size and shape. Objects spatial and perceptual features need to be integrated during grasping, but those features are analyzed in two anatomically distinct neural pathways. The anterior intraparietal sulcus (aIPS) might support the integration of those features. We combine transcranial magnetic stimulation (TMS) interference, EEG recordings, and psychophysical methods to test aIPS causal contributions to sensorimotor integration, characterizing the dynamics of those contributions during motor planning. Human subjects performing grasping movements were provided with visual information about a target object, namely spatial and pictorial cues, whose availability and information value were independently modulated on each trial. Maximally informative visual cues, irrespective of their spatial or perceptual nature, led to enhanced motor preparatory activity early during movement planning, and to stronger spatial congruency between finger trajectories and target object. Disturbing aIPS activity with single-pulse TMS within 200 ms after object presentation reduced those electrophysiological and behavioral indices of enhanced motor planning. TMS interference with aIPS also disturbed subjects ability to use learned object knowledge during motor planning. These results indicate that aIPS is necessary for the fast generation of a new motor plan on the basis of both spatial and pictorial cues. Furthermore, as learned object knowledge becomes available, aIPS comes to strongly depend on this prior information for structuring the motor plan.

Reduced Serotonin Transporter Availability Decreases Prefrontal Control of the Amygdala

After a threatening event, the risk of developing social psychopathologies is increased in short-allele (s) carriers of the serotonin transporter gene. The amygdala becomes overresponsive to emotional stimuli, an effect that could be driven by local hypersensitivity or by reduced prefrontal regulation. This study distinguishes between these two hypotheses by using dynamic causal modeling of fMRI data acquired in a preselected cohort of human s-carriers and homozygous long-allele carriers. Increased amygdala activity in s-carriers originates from reduced prefrontal inhibitory regulation when social emotional behavior needs to be controlled, suggesting a mechanism for increased vulnerability to psychopathologies.

Hierarchical Organization of Parietofrontal Circuits during Goal-Directed Action

Two parietofrontal networks share the control of goal-directed movements: a dorsomedial circuit that includes the superior parieto-occipital sulcus (sPOS) and a dorsolateral circuit comprising the anterior intraparietal sulcus (aIPS). These circuits are thought to independently control either reach and grip components (a functional dissociation), or planning and execution phases of grasping movements (a temporal dissociation). However, recent evidence of functional and temporal overlap between these circuits has undermined those models. Here, we test an alternative model that subsumes previous accounts: the dorsolateral and dorsomedial circuits operate at different hierarchical levels, resulting in functional and temporal dependencies between their computations. We asked human participants to grasp a visually presented object, manipulating movement complexity by varying object slant. We used concurrent single-pulse transcranial magnetic stimulation and electroencephalography (TMS-EEG) to probe and record neurophysiological activity in the two circuits. Changes in alpha-band oscillations (8–12 Hz) characterized the effects of task manipulations and TMS interferences over aIPS and sPOS. Increasing the complexity of the grasping movement was accompanied by alpha-suppression over dorsomedial parietofrontal regions, including sPOS, during both planning and execution stages. TMS interference over either aIPS or sPOS disrupted this index of dorsomedial computations; early when aIPS was perturbed, later when sPOS was perturbed, indicating that the dorsomedial circuit is temporally dependent on aIPS. TMS over sPOS enhanced alpha-suppression in inferior parietal cortex, indicating that the dorsolateral circuit can compensate for a transient sPOS perturbation. These findings suggest that both circuits specify the same grasping parameters, with dorsomedial computations depending on dorsolateral contributions.

Book review: Foraging with a prefrontal cortex makes all the difference

My cat is learning to catch squirrels in the back garden. Its a painfully slow process. He seems to be trying every available technique, improving step by step. Hes tried sitting near the house and charging down the garden when a squirrel appeared, only for the squirrel to spot him and dash off. Hes tried assaulting the squirrel when it came down the tree, only to find out that squirrels climb faster than cats. He doesnt seem to have an overview of the situation, grasping that his best strategy is to hide near the back fence, the only place where he can sneak up on the squirrel and cut off its escape route. Why isnt he capable of that seemingly simple strategic inference? A new book by Passingham and Wise (2012) provides a possible answer: because he doesnt have the large, primate prefrontal cortex (PFC). n nPassingham and Wise (2012) set out to understand the organization and function of the primate PFC by combining evolutionary and ecological perspectives. Large parts of PFC, and specifically those with a granular cortical layer, are a primate invention. The authors argue that the development of these areas reflects the changes in foraging niches encountered during the evolution of the primate order. n nThere is a large body of work relating aspects of brain evolution to specific ecological variables, most notably foraging habits (Clutton-Brock and Harvey, 1980) and social organization (Dunbar, 1998). However, these studies have mostly focused on the relative size of the entire brain or neocortex. In contrast, work dealing with more detailed brain anatomy has tended to focus less on the evolutionary context. The unique contribution of this book is that it combines the two approaches without compromises, focusing on a detailed reconstruction of the ecological challenges encountered by the primate brain and the anatomical information that provides avenues to understanding how these challenges have been met.