Neural Correlates of Animacy Attribution Include Neocerebellum in Healthy Adults.
ABSTRACT: Recent work suggests that biological motion perception is supported by interactions between posterior superior temporal sulcus (pSTS) and regions of the posterior lobe of the cerebellum. However, insufficient attention has been given to cerebellar contributions to most other social cognitive functions, including ones that rely upon the use of biological motion cues for making mental inferences. Here, using adapted Heider and Simmel stimuli in a passive-viewing paradigm, we present functional magnetic resonance imaging evidence detailing cerebellar contributions to animacy attribution processes in healthy adults. We found robust cerebellar activity associated with viewing animate versus random movement in hemispheric lobule VII bilaterally as well as in vermal and paravermal lobule IX. Stronger activity in left Crus I and lobule VI was associated with a greater tendency to describe the stimuli in social-affective versus motion-related terms. Psychophysiological interaction analysis indicated preferential effective connectivity between right pSTS and left Crus II during the viewing of animate than random stimuli, controlling for individual variance in social attributions. These findings indicate that lobules VI, VII, and IX participate in social functions even when no active response is required. This cerebellar activity may also partially explain individual differences in animacy attribution.
Project description:Decades of research have demonstrated that a region of the right fusiform gyrus (FG) and right posterior superior temporal sulcus (pSTS) responds preferentially to static faces and biological motion, respectively. Despite this view, both regions activate in response to both stimulus categories and to a range of other stimuli, such as goal-directed actions, suggesting that these regions respond to characteristics of animate agents more generally. Here we propose a neural model for animacy detection composed of processing streams that are initially differentially sensitive to cues signaling animacy, but that ultimately act in concert to support reasoning about animate agents. We use dynamic causal modeling, a measure of effective connectivity, to demonstrate that the directional flow of information between the FG and pSTS is initially dependent on the characteristics of the animate agent presented, a key prediction of our proposed network for animacy detection.
Project description:The right posterior superior temporal sulcus (pSTS) is a neural region involved in assessing the goals and intentions underlying the motion of social agents. Recent research has identified visual cues, such as chasing, that trigger animacy detection and intention attribution. When readily available in a visual display, these cues reliably activate the pSTS. Here, using functional magnetic resonance imaging, we examined if attributing intentions to random motion would likewise engage the pSTS. Participants viewed displays of four moving circles and were instructed to search for chasing or mirror-correlated motion. On chasing trials, one circle chased another circle, invoking the percept of an intentional agent; while on correlated motion trials, one circle's motion was mirror reflected by another. On the remaining trials, all circles moved randomly. As expected, pSTS activation was greater when participants searched for chasing vs correlated motion when these cues were present in the displays. Of critical importance, pSTS activation was also greater when participants searched for chasing compared to mirror-correlated motion when the displays in both search conditions were statistically identical random motion. We conclude that pSTS activity associated with intention attribution can be invoked by top-down processes in the absence of reliable visual cues for intentionality.
Project description:Posterior superior temporal sulcus (pSTS) is specialized for interpreting perceived human actions, and disruptions to its function occur in autism spectrum disorder (ASD). Here we consider the role of Crus I of neocerebellum in supporting pSTS function. Research has associated Crus I activity with imitation and biological motion perception, and neocerebellum is theorized to coordinate activity among cerebral sites more generally. Moreover, cerebellar abnormalities have been associated with ASD. We hypothesized that disordered Crus I-pSTS interactions could predict social deficits in ASD. 15 high functioning adolescents with ASD and 15 same-age comparison youth participated in an fMRI imitation paradigm; ratings of mentalizing ability were collected via parent report. We predicted that stronger Crus I-pSTS interactions would be associated with better mentalizing ability. Consistent with these hypotheses, stronger psychophysiological interactions between Crus I and right pSTS were associated with greater mentalizing ability among adolescents with ASD. Whole-brain analyses also indicated that typically developing youth recruited right inferior frontal gyrus, left pSTS, medial occipital regions, and precuneus more strongly during imitation than did youth with ASD. Overall, these results indicate that variability in neocerebellar interactions with key cortical social brain sites may help explain individual differences in social perceptual outcomes in ASD.
Project description:Biological agents are the most complex systems humans have to model and predict. In predictive coding, high-level cortical areas inform sensory cortex about incoming sensory signals, a comparison between the predicted and actual sensory feedback is made, and information about unpredicted sensory information is passed forward to higher-level areas. Predictions about animate motion - relative to inanimate motion - should result in prediction error and increase signal passing from lower level sensory area MT+/V5, which is responsive to all motion, to higher-order posterior superior temporal sulcus (pSTS), which is selectively activated by animate motion. We tested this hypothesis by investigating effective connectivity in a large-scale fMRI dataset from the Human Connectome Project. 132 participants viewed animations of triangles that were designed to move in a way that appeared animate (moving intentionally), or inanimate (moving in a mechanical way). We found that forward connectivity from V5 to the pSTS increased, and inhibitory self-connection in the pSTS decreased, when viewing intentional motion versus inanimate motion. These prediction errors associated with animate motion may be the cause for increased attention to animate stimuli found in previous studies.
Project description:Cognitive and social capacities require postnatal experience, yet the pathways by which experience guides development are unknown. Here we show that the normal development of motor and nonmotor capacities requires cerebellar activity. Using chemogenetic perturbation of molecular layer interneurons to attenuate cerebellar output in mice, we found that activity of posterior regions in juvenile life modulates adult expression of eyeblink conditioning (paravermal lobule VI, crus I), reversal learning (lobule VI), persistive behavior and novelty-seeking (lobule VII), and social preference (crus I/II). Perturbation in adult life altered only a subset of phenotypes. Both adult and juvenile disruption left gait metrics largely unaffected. Contributions to phenotypes increased with the amount of lobule inactivated. Using an anterograde transsynaptic tracer, we found that posterior cerebellum made strong connections with prelimbic, orbitofrontal, and anterior cingulate cortex. These findings provide anatomical substrates for the clinical observation that cerebellar injury increases the risk of autism.
Project description:Primates are highly attuned not just to social characteristics of individual agents, but also to social interactions between multiple agents. Here we report a neural correlate of the representation of social interactions in the human brain. Specifically, we observe a strong univariate response in the posterior superior temporal sulcus (pSTS) to stimuli depicting social interactions between two agents, compared with (<i>i</i>) pairs of agents not interacting with each other, (<i>ii</i>) physical interactions between inanimate objects, and (<i>iii</i>) individual animate agents pursuing goals and interacting with inanimate objects. We further show that this region contains information about the nature of the social interaction-specifically, whether one agent is helping or hindering the other. This sensitivity to social interactions is strongest in a specific subregion of the pSTS but extends to a lesser extent into nearby regions previously implicated in theory of mind and dynamic face perception. This sensitivity to the presence and nature of social interactions is not easily explainable in terms of low-level visual features, attention, or the animacy, actions, or goals of individual agents. This region may underlie our ability to understand the structure of our social world and navigate within it.
Project description:To examine the cerebellar contribution to human spatial navigation we used functional magnetic resonance imaging and virtual reality. Our findings show that the sensory-motor requirements of navigation induce activity in cerebellar lobules and cortical areas known to be involved in the motor loop and vestibular processing. By contrast, cognitive aspects of navigation mainly induce activity in a different cerebellar lobule (VIIA Crus I). Our results demonstrate a functional link between cerebellum and hippocampus in humans and identify specific functional circuits linking lobule VIIA Crus I of the cerebellum to medial parietal, medial prefrontal, and hippocampal cortices in nonmotor aspects of navigation. They further suggest that Crus I belongs to 2 nonmotor loops, involved in different strategies: place-based navigation is supported by coherent activity between left cerebellar lobule VIIA Crus I and medial parietal cortex along with right hippocampus activity, while sequence-based navigation is supported by coherent activity between right lobule VIIA Crus I, medial prefrontal cortex, and left hippocampus. These results highlight the prominent role of the human cerebellum in both motor and cognitive aspects of navigation, and specify the cortico-cerebellar circuits by which it acts depending on the requirements of the task.
Project description:The cognitive dysmetria theory of psychotic disorders posits that cerebellar circuit abnormalities give rise to difficulties coordinating motor and cognitive functions. However, brain activation during cerebellar-mediated tasks is understudied in schizophrenia. Accordingly, this study examined whether individuals with schizophrenia have diminished neural activation compared to controls in key regions of the delay eyeblink conditioning (dEBC) cerebellar circuit (eg, lobule VI) and cerebellar regions associated with cognition (eg, Crus I). Participants with schizophrenia-spectrum disorders (<i>n</i> = 31) and healthy controls (<i>n</i> = 43) underwent dEBC during functional magnetic resonance imaging (fMRI). Images were normalized using the Spatially Unbiased Infratentorial Template (SUIT) of the cerebellum and brainstem. Activation contrasts of interest were "early" and "late" stages of paired tone and air puff trials minus unpaired trials. Preliminary whole brain analyses were conducted, followed by cerebellar-specific SUIT and region of interest (ROI) analyses of lobule VI and Crus I. Correlation analyses were conducted between cerebellar activation, neuropsychological test scores, and psychotic symptom scores. In controls, the largest clusters of cerebellar activation peaked in lobule VI during early dEBC and Crus I during late dEBC. The schizophrenia group showed robust cortical activation to unpaired trials but no significant conditioning-related cerebellar activation. Crus I ROI activation during late dEBC was greater in the control than schizophrenia group. Greater Crus I activation correlated with higher working memory scores in the full sample and lower positive psychotic symptom severity in schizophrenia. Findings indicate functional cerebellar abnormalities in schizophrenia which relate to psychotic symptoms, lending direct support to the cognitive dysmetria framework.
Project description:Simple geometric shapes moving in a self-propelled manner, and violating Newtonian laws of motion by acting against gravitational forces tend to induce a judgement that an object is animate. Objects that change their motion only due to external causes are more likely judged as inanimate. How the developing brain is employed in the perception of animacy in early ontogeny is currently unknown. The aim of this study was to use ERP techniques to determine if the negative central component (Nc), a waveform related to attention allocation, was differentially affected when an infant observed animate or inanimate motion. Short animated movies comprising a marble moving along a marble run either in an animate or an inanimate manner were presented to 15 infants who were 9 months of age. The ERPs were time-locked to a still frame representing animate or inanimate motion that was displayed following each movie. We found that 9-month-olds are able to discriminate between animate and inanimate motion based on motion cues alone and most likely allocate more attentional resources to the inanimate motion. The present data contribute to our understanding of the animate-inanimate distinction and the Nc as a correlate of infant cognitive processing.