Brain regions involved in observing and trying to interpret dog behaviour

Humans and dogs have interacted for millennia. As a result, humans (and especially dog owners) sometimes try to interpret dog behaviour. While there is extensive research on the brain regions that are involved in mentalizing about other peoples' behaviour, surprisingly little is known of whether we use these same brain regions to mentalize about animal behaviour. In this fMRI study we investigate whether brain regions involved in mentalizing about human behaviour are also engaged when observing dog behaviour. Here we show that these brain regions are more engaged when observing dog behaviour that is difficult to interpret compared to dog behaviour that is easy to interpret. Interestingly, these results were not only obtained when participants were instructed to infer reasons for the behaviour but also when they passively viewed the behaviour, indicating that these brain regions are activated by spontaneous mentalizing processes

Moving higher and higher: imitators' movements are sensitive to observed trajectories regardless of action rationality

Humans sometimes perform actions which, at least superficially, appear suboptimal to the goal they are trying to achieve. Despite being able to identify these irrational actions from an early age, humans display a curious tendency to copy them. The current study recorded participants' movements during an established imitation task and manipulated the rationality of the observed action in two ways. Participants observed videos of a model point to a series of targets with either a low, high or 'superhigh' trajectory either in the presence or absence of obstacles between her targets. The participants' task was to watch which targets the model pointed to and then point to the same targets on the table in front of them. There were no obstacles between the participants' targets. Firstly, we found that the peak height of participants' movements between their targets was sensitive to the height of the model's movements, even in the 'superhigh' condition where the model's action was rated as irrational. Secondly, participants showed obstacle priming-the peak height of participants' movements was higher after having observed the model move over obstacles to reach her targets, compared to when there were no obstacles between her targets. This suggests that participants code the environment of co-actors into their own motor programs, even when this compromises the efficiency of their own movements. We discuss the implications of our findings in terms of theories of imitation and obstacle priming

The Graded Change in Connectivity across the Ventromedial Prefrontal Cortex Reveals Distinct Subregions.

The functional heterogeneity of the ventromedial prefrontal cortex (vmPFC) suggests it may include distinct functional subregions. To date these have not been well elucidated. Regions with differentiable connectivity (and as a result likely dissociable functions) may be identified using emergent data-driven approaches. However, prior parcellations of the vmPFC have only considered hard splits between distinct regions, although both hard and graded connectivity changes may exist. Here we determine the full pattern of change in structural and functional connectivity across the vmPFC for the first time and extract core distinct regions. Both structural and functional connectivity varied along a dorsomedial to ventrolateral axis from relatively dorsal medial wall regions to relatively lateral basal orbitofrontal cortex. The pattern of connectivity shifted from default mode network to sensorimotor and multimodal semantic connections. This finding extends the classical distinction between primate medial and orbital regions by demonstrating a similar gradient in humans for the first time. Additionally, core distinct regions in the medial wall and orbitofrontal cortex were identified that may show greater correspondence to functional differences than prior hard parcellations. The possible functional roles of the orbitofrontal cortex and medial wall are discussed.This work was supported by a doctoral prize from the Engineering and Physical Sciences Research Council and a British Academy Postdoctoral Fellowship (pf170068) to RLJ, a studentship from the BBSRC (BB/J014478/1) to CJB, and programme grants from the Medical Research Council (MR/J004146/1 & MR/R023883/1) to MALR

The graded change in connectivity across the ventromedial prefrontal cortex reveals distinct subregions

The functional heterogeneity of the ventromedial prefrontal cortex (vmPFC) suggests it may include distinct functional subregions. To date these have not been well elucidated. Regions with differentiable connectivity (and as a result likely dissociable functions) may be identified using emergent data-driven approaches. However, prior parcellations of the vmPFC have only considered hard splits between distinct regions, although both hard and graded connectivity changes may exist. Here we determine the full pattern of change in structural and functional connectivity across the vmPFC for the first time and extract core distinct regions. Both structural and functional connectivity varied along a dorsomedial to ventrolateral axis from relatively dorsal medial wall regions to relatively lateral basal orbitofrontal cortex. The pattern of connectivity shifted from default mode network to sensorimotor and multimodal semantic connections. This finding extends the classical distinction between primate medial and orbital regions by demonstrating a similar gradient in humans for the first time. Additionally, core distinct regions in the medial wall and orbitofrontal cortex were identified that may show greater correspondence to functional differences than prior hard parcellations. The possible functional roles of the orbitofrontal cortex and medial wall are discussed.peer-reviewe

The Psychobiology of Conscience: Signatures in Brain Regions of Interest

OBJECTIVES: 1) to highlight studies in the last eight years in which functional magnetic resonance imaging or other neuroimaging techniques have been employed in identifying brain activities as putative correlates of various TASKS proposed to represent essential MORAL PSYCHOLOGICAL FUNCTIONS and 2) to consider how NEUROIMAGING STUDIES of CONSCIENCE FUNCTIONAL TASKS might be conducted which provide more depth and meaning in future moral psychobiological investigation. METHOD: Brief descriptions of the principles and caveats of interpreting findings from NEUROIMAGING are provided. A GLOSSARY OF TERMS derived from cognitive sciences including neuropsychology and developmental psychology is presented. These terms, it is suggested, are necessary but not sufficient in understanding the DOMAINS OF CONSCIENCE. Existing NEUROIMAGING STUDIES of putative MORAL PSYCHOLOGICAL FUNCTIONAL TASKS that (at least nominally) address aspects of each CONSCIENCE DOMAIN are reviewed. These STUDIES are organized according to the following subtitles (with the CONSCIENCE DOMAIN of concern identified parenthetically): MORAL COGNITION: MORAL JUDGMENT AND VALENCE (CONSCIENCE DOMAIN: VALUATION), EMPATHY (CONSCIENCE DOMAIN: MORALIZED ATTACHMENT), MORAL EMOTIONS (CONSCIENCE DOMAIN: MORAL EMOTIONAL RESPONSIVENESS), and SELF CONTROL (CONSCIENCE DOMAIN: MORAL VOLITION). No existing NEUROIMAGING STUDIES clearly correspond to the anchor domain, CONCEPTUALIZATION OF CONSCIENCE. The CONSCIENCE DOMAINS are briefly characterized with reference to the empirical research supporting each. CONCLUSIONS: In the last several years, a number of intriguing findings have emerged from NEURO-IMAGING STUDIES relevant to putative MORAL PSYCHOLOGICAL FUNCTIONAL TASKS. However, in addition to caveats attaching to any attribution of activity to neurological structures and their connections based upon signals captured via NEURO-IMAGING, serious concerns also arise regarding the validity of the TASKS currently employed in these studies as truly representative of CONSCIENCE FUNCTIONS. Instruments designed to inquire into relevant CONSCIENCE DOMAINS are put forward. Complementary TASKS more sensitive to each CONSCIENCE DOMAIN are imagined and offered for consideration as ways to provide more depth and meaning to future NEUROIMAGING STUDIES OF CONSCIENCE

The Neural Basis of Mentalizing Deficits Experienced by Adults with Autism Spectrum Disorder

Adults with autism spectrum disorder (ASD) are widely regarded to exhibit difficulties inferring the internal states of others; known as ‘mentalizing’. However, the existing literature is inconsistent regarding the nature of the mentalizing difficulties experienced by adults with ASD. Two neural systems; the mirror neuron system (MNS) and the mentalizing system, are both thought to play important roles in inferring others’ internal states from their actions but the precise roles of these systems and the nature of the interaction between them are unknown. The aim of this thesis was to explore the nature of mentalizing deficits associated with ASD, delineate between existing models of MNS involvement in mentalizing and identify the neural basis of mentalizing difficulties associated with ASD. The first empirical chapter presents two behavioural experiments which found adults with ASD were impaired at explicitly inferring the intentions of others from their actions. The second empirical chapter presents a transcranial magnetic stimulation (TMS) experiment which identified mentalizing-induced modulation of MNS activity, at the end of observed actions, in typically developing participants. The third empirical chapter presents an experiment which used TMS and electroencephalography (EEG) to measure MNS activation in adults with ASD when mentalizing and found higher levels of autistic traits predicted lower right-lateralised MNS activity. The final empirical chapter presents a functional magnetic resonance imaging (fMRI) experiment which identified higher levels of autistic traits predicted reduced functional connectivity between the MNS and the mentalizing system. Collectively, these data suggest that connectivity between the MNS and the mentalizing system is higher when inferring intentions of others from their actions, the interaction between the two systems may be best conceptualised within a predictive coding framework and reduced connectivity between these systems may underlie the mentalizing difficulties adults with ASD experience

Sophisticated Deception in Junior Middle School Students: An ERP Study

Sophisticated deception refers to the deception of others based on inferences of their mental states (e.g., answering honestly when inferring that the other will not believe their answer). Studying the brain mechanism of sophisticated deception in junior middle school students can provide physiological evidence for deception detection and deceptive ability measurement. Sixteen junior middle school students were asked to engage in different trial types (i.e., instructed truth/lie and chosen truth/lie), during which we recorded their response times (RT) along with electroencephalographic data to calculate event-related potentials (ERPs). We observed significant differences in amplitude [N2, P3, N450, and medial frontal negativity (MFN)] between chosen reactions (sophisticated deception and simple deception) and instructed reactions (instructed truth and instructed lie) in both the stimulus presentation and feedback stages. In the former, the task scores of participants in the chosen condition were significantly and positively correlated with the N2 amplitude over the central brain area during sophisticated deception. In the latter, the task scores of participants in the chosen condition were negatively correlated with the MFN amplitude over the left frontal and left frontocentral regions. Overall, deception intention, rather than simply making counterfactual statements, appears to underlie the increased demand for cognitive control in deceivers. This can be attributed to deceivers’ need to strongly consider their opponent’s mental state—the better the deceivers’ deceptive ability, the more they will make conjectures about the mental state of their opponent with sophisticated deception and monitor conflict; the less conflict they experience while answering honestly with the intention to deceive, the more conflict may arise when the results of their deception are inconsistent with these conjectures

Perceptual Teleology: Expectations of Action Efficiency Bias Social Perception

No embargo required.Primates interpret conspecific behaviour as goal-directed and expect others to achieve goals by the most efficient means possible. While this teleological stance is prominent in evolutionary and developmental theories of social cognition, little is known about the underlying mechanisms. In predictive models of social cognition, a perceptual prediction of an ideal efficient trajectory would be generated from prior knowledge against which the observed action is evaluated, distorting the perception of unexpected inefficient actions. To test this, participants observed an actor reach for an object with a straight or arched trajectory on a touch screen. The actions were made efficient or inefficient by adding or removing an obstructing object. The action disappeared mid-trajectory and participants touched the last seen screen position of the hand. Judgements of inefficient actions were biased towards the efficient prediction (straight trajectories upward to avoid the obstruction, arched trajectories downward towards the target). These corrections increased when the obstruction's presence/absence was explicitly acknowledged, and when the efficient trajectory was explicitly predicted. Additional supplementary experiments demonstrated that these biases occur during ongoing visual perception and/or immediately after motion offset. The teleological stance is at least partly perceptual, providing an ideal reference trajectory against which actual behaviour is evaluated.</jats:p

Neural and motor basis of inter-individual interactions

The goal of my Ph.D. work was to investigate the behavioral markers and the brain activities responsible for the emergence of sensorimotor communication. Sensorimotor communication can be defined as a form of communication consisting into flexible exchanges based on bodily signals, in order to increase the efficiency of the inter-individual coordination. For instance, a soccer player carving his movements to inform another player about his intention. This form of interaction is highly dependent of the motor system and the ability to produce appropriate movements but also of the ability of the partner to decode these cues. To tackle these facets of human social interaction, we approached the complexity of the problem by splitting my research activities into two separate lines of research. First, we pursued the examination of motor-based humans\u2019 capability to perceive and \u201cread\u201d other\u2019s behaviors in focusing on single-subject experiment. The discovery of mirror neurons in monkey premotor cortex in the early nineties (di Pellegrino et al. 1992) motivated a number of human studies on this topic (Rizzolatti and Craighero 2004). The critical finding was that some ventral premotor neurons are engaged during visual presentation of actions performed by conspecifics. More importantly, those neurons were shown to encode also the actual execution of similar actions (i.e. irrespective of who the acting individual is). This phenomenon has been highly investigated in humans by using cortical and cortico-spinal measures (for review see, fMRI: Molenberghs, Cunnington, and Mattingley 2012; TMS: Naish et al. 2014; EEG: Pineda 2008). During single pulse TMS (over the primary motor cortex), the amplitude of motor evoked potentials (MEPs) provides an index of corticospinal recruitment. During action observation the modulation of this index follow the expected changes during action execution (Fadiga et al. 1995). However, dozens of studies have been published on this topic and revealed important inconsistencies. For instance, MEPs has been shown to be dependent on observed low-level motor features (e.g. kinematic features or electromyography temporal coupling; Gangitano, Mottaghy, and Pascual-Leone 2001; Borroni et al. 2005; Cavallo et al. 2012) as well as high level movement properties (e.g. action goals; Cattaneo et al. 2009; Cattaneo et al. 2013). Furthermore, MEPs modulations do not seem to be related to the observed effectors (Borroni and Baldissera 2008; Finisguerra et al. 2015; Senna, Bolognini, and Maravita 2014), suggesting their independence from low-level movement features. These contradictions call for new paradigms. Our starting hypothesis here is that the organization and function of the mirror mechanism should follow that of the motor system during action execution. Hence, we derived three action observation protocols from classical motor control theories: 1) The first study was motivated by the fact that motor redundancy in action execution do not allow the presence of a one-to-one mapping between (single) muscle activation and action goals. Based on that, we showed that the effect of action observation (observation of an actor performing a power versus a precision grasp) are variable at the single muscle level (MEPs; motor evoked potentials) but robust when evaluating the kinematic of TMS-evoked movements. Considering that movements are based on the coordination of multiple muscle activations (muscular synergies), MEPs may represent a partial picture of the real corticospinal activation. Inversely, movement kinematics is both the final functional byproduct of muscles coordination and the sole visual feedback that can be extracted from action observation (i.e. muscle recruitment is not visible). We conclude that TMS-evoked kinematics may be more reliable in representing the state of the motor system during action observation. 2) In the second study, we exploited the inter-subject variability inherent to everyday whole-body human actions, to evaluate the link between individual motor signatures (or motor styles) and other\u2019s action perception. We showed no group-level effect but a robust correlation between the individual motor signature recorded during action execution and the subsequent modulations of corticospinal excitability during action observation. However, results were at odds with a strict version of the direct matching hypothesis that would suggest the opposite pattern. In fact, the more the actor\u2019s movement was similar to the observer\u2019s individual motor signature, the smaller was the MEPs amplitude, and vice versa. These results conform to the predictive coding hypothesis, suggesting that during AO, the motor system compares our own way of doing the action (individual motor signature) with the action displayed on the screen (actor\u2019s movement). 3) In the third study, we investigated the neural mechanisms underlying the visual perception of action mistakes. According to a strict version of the direct matching hypothesis, the observer should potentially reproduce the neural activation present during the actual execution of action errors (van Schie et al. 2004). Here, instead of observing an increase of cortical inhibition, we showed an early (120 ms) decrease of intracortical inhibition (short intracortical inhibition) when a mismatch was present between the observed action (erroneous) and the observer\u2019s expectation. As proposed by the predictive coding framework, the motor system may be involved in the generation of an error signal potentially relying on an early decrease of intracortical inhibition within the corticomotor system. The second line of research aimed at the investigation of how sensorimotor communication flows between agents engaged in a complementary action coordination task. In this regard, measures of interest where related to muscle activity and/or kinematics as the recording of TMS-related indexes would be too complicated in a joint-action scenario. 1) In the first study, we exploited the known phenomenon of Anticipatory Postural Adjustments (APAs). APAs refers to postural adjustments made in anticipation of a self- or externally-generated disturbance in order to cope for the predicted perturbation and stabilize the current posture. Here we examined how observing someone else lifting an object we hold can affect our own anticipatory postural adjustments of the arm. We showed that the visual information alone (joint action condition), in the absence of efference copy (present only when the subject is unloading by himself the object situated on his hand), were not sufficient to fully deploy the needed anticipatory muscular activations. Rather, action observation elicited a dampened APA response that is later augmented by the arrival of tactile congruent feedback. 2) In a second study, we recorded the kinematic of orchestra musicians (one conductor and two lines of violinists). A manipulation was added to perturb the normal flow of information conveyed by the visual channel. The first line of violinist where rotated 180\ub0, and thus faced the second line. Several techniques were used to extract inter-group (Granger Causality method) and intra-group synchronization (PCA for musicians and autoregression for conductors). The analyses were directed to two kinematic features, hand and head movements, which are central for functionally different action. The hand is essential for instrumental actions, whereas head movements encode ancillary expressive actions. During the perturbation, we observed a complete reshaping of the whole patterns of communication going in the direction of a distribution of the leadership between conductor and violinists, especially for what regards head movements. In fact, in the perturbed condition, the second line acts as an informational hub connecting the first line to the conductor they no longer can see. This study evidences different forms of communications (coordination versus synchronization) flowing via different channels (ancillary versus instrumental) with different time-scales