Robert P. Spunt

Identifying the what, why, and how of an observed action: An fmri study of mentalizing and mechanizing during action observation

Humans commonly understand the unobservable mental states of others by observing their actions. Embodied simulation theories suggest that this ability may be based in areas of the fronto-parietal mirror neuron system, yet neuroimaging studies that explicitly investigate the human ability to draw mental state inferences point to the involvement of a “mentalizing” system consisting of regions that do not overlap with the mirror neuron system. For the present study, we developed a novel action identification paradigm that allowed us to explicitly investigate the neural bases of mentalizing observed actions. Across repeated viewings of a set of ecologically valid video clips of ordinary human actions, we manipulated the extent to which participants identified the unobservable mental states of the actor (mentalizing) or the observable mechanics of their behavior (mechanizing). Although areas of the mirror neuron system did show an enhanced response during action identification, its activity was not significantly modulated by the extent to which the observers identified mental states. Instead, several regions of the mentalizing system, including dorsal and ventral aspects of medial pFC, posterior cingulate cortex, and temporal poles, were associated with mentalizing actions, whereas a single region in left lateral occipito-temporal cortex was associated with mechanizing actions. These data suggest that embodied simulation is insufficient to account for the sophisticated mentalizing that human beings are capable of while observing another and that a different system along the cortical midline and in anterior temporal cortex is involved in mentalizing an observed action.

Evidence for social working memory from a parametric functional MRI study

Keeping track of various amounts of social cognitive information, including peoples mental states, traits, and relationships, is fundamental to navigating social interactions. However, to date, no research has examined which brain regions support variable amounts of social information processing (“social load”). We developed a social working memory paradigm to examine the brain networks sensitive to social load. Two networks showed linear increases in activation as a function of increasing social load: the medial frontoparietal regions implicated in social cognition and the lateral frontoparietal system implicated in nonsocial forms of working memory. Of these networks, only load-dependent medial frontoparietal activity was associated with individual differences in social cognitive ability (trait perspective-taking). Although past studies of nonsocial load have uniformly found medial frontoparietal activity decreases with increasing task demands, the current study demonstrates these regions do support increasing mental effort when such effort engages social cognition. Implications for the etiology of clinical disorders that implicate social functioning and potential interventions are discussed.

The Busy Social Brain Evidence for Automaticity and Control in the Neural Systems Supporting Social Cognition and Action Understanding

Much social-cognitive processing is believed to occur automatically; however, the relative automaticity of the brain systems underlying social cognition remains largely undetermined. We used functional MRI to test for automaticity in the functioning of two brain systems that research has indicated are important for understanding other people’s behavior: the mirror neuron system and the mentalizing system. Participants remembered either easy phone numbers (low cognitive load) or difficult phone numbers (high cognitive load) while observing actions after adopting one of four comprehension goals. For all four goals, mirror neuron system activation showed relatively little evidence of modulation by load; in contrast, the association of mentalizing system activation with the goal of inferring the actor’s mental state was extinguished by increased cognitive load. These results support a dual-process model of the brain systems underlying action understanding and social cognition; the mirror neuron system supports automatic behavior identification, and the mentalizing system supports controlled social causal attribution.

Dissociating Modality-Specific and Supramodal Neural Systems for Action Understanding

The neural basis of action understanding in humans remains disputed, with some research implicating the putative mirror neuron system (MNS) and some a mentalizing system (MZS) for inferring mental states. The basis for this dispute may be that action understanding is a heterogeneous construct: actions can be understood from sensory information about body movements or from language about action, and with the goal of understanding the implementation (“how”) or motive (“why”) of an action. Although extant research implicates the MNS in understanding implementation and the MZS in understanding motive, it remains unknown to what extent these systems subserve modality-specific or supramodal functions in action understanding. While undergoing fMRI, 21 volunteers considered the implementation (“How is she doing it?”) and motive (“Why is she doing it?”) for actions presented in video or text. Bilateral parietal and right frontal areas of the MNS showed a modality-specific association with perceiving actions in videos, while left-hemisphere MNS showed a supramodal association with understanding implementation. Largely left-hemisphere MZS showed a supramodal association with understanding motive; however, connectivity among the MZS and MNS during the inference of motive was modality specific, being significantly stronger when motive was understood from actions in videos compared to text. These results support a tripartite model of MNS and MZS contributions to action understanding, where distinct areas of the MNS contribute to action perception (“perceiving what”) and the representation of action implementation (“knowing how”), while the MZS supports an abstract, modality-independent representation of the mental states that explain action performance (“knowing why”).

Dissociable Neural Systems Support Retrieval of How and Why Action Knowledge

In everyday discourse, people typically represent actions in one of two ways: how they are performed or why they are performed. In the present study, we determined the neural systems that support these natural modes of representing actions. Participants underwent functional magnetic resonance imaging while identifying how and why people perform various familiar actions. Identifying how actions are performed produced activity in premotor areas that support the execution of actions and in higher-order visual areas that support the perception of action-related objects; this finding supports an embodied view of action knowledge. However, identifying why actions are performed preferentially engaged areas of the brain associated with representing and reasoning about mental states; these areas were right temporoparietal junction, precuneus, dorsomedial prefrontal cortex, and posterior superior temporal sulcus. Our results suggest that why action knowledge is not sufficiently constituted by information in motor and visual systems, but requires a system for representing states of mind, which do not have reliable motor correlates or visual appearance.

The phenomenology of error processing: The dorsal acc response to stop-signal errors tracks reports of negative affect

A reliable observation in neuroimaging studies of cognitive control is the response of dorsal ACC (dACC) to events that demand increased cognitive control (e.g., response conflicts and performance errors). This observation is apparently at odds with a comparably reliable association of the dACC with the subjective experience of negative affective states such as pain, fear, and anxiety. Whereas “affective” associates of the dACC are based on studies that explicitly manipulate and/or measure the subjective experience of negative affect, the “cognitive” associates of dACC are based on studies using tasks designed to manipulate the demand for cognitive control, such as the Stroop, flanker, and stop-signal tasks. Critically, extant neuroimaging research has not systematically considered the extent to which these cognitive tasks induce negative affective experiences and, if so, to what extent negative affect can account for any variance in the dACC response during task performance. While undergoing fMRI, participants in this study performed a stop-signal task while regularly reporting their experience of performance on several dimensions. We observed that within-subject variability in the dACC response to stop-signal errors tracked changes in subjective frustration throughout task performance. This association remained when controlling for within-subject variability in subjective reports of cognitive engagement and several performance-related variables indexing task difficulty. These results fit with existing models characterizing the dACC as a hub for monitoring ongoing behavior and motivating adjustments when necessary and further emphasize that such a function may be linked to the subjective experience of negative affect.

Ascribing beliefs to ingroup and outgroup political candidates: neural correlates of perspective-taking, issue importance and days until the election

We used the five weeks leading up to the 2008 presidential election as a backdrop to examine the ways that the brain processes attitudes and beliefs under different circumstances. We examined individual differences in personal issue importance and trait perspective-taking, as well as the temporal context in which attitude representation took place (i.e. number of days until the election). Finally, we examined the extent to which similar or dissimilar processes were recruited when considering the attitudes of political ingroup and outgroup candidates. Brain regions involved in social cognition and theory of mind, and to a lesser extent the limbic system, were modulated by these factors. Higher issue importance led to greater recruitment of neural regions involved in social cognition, across target perspectives. Higher trait perspective-taking was also associated with greater recruitment of several regions involved in social cognition, but differed depending on target perspective; greater activity was observed in prefrontal regions associated with social cognition when considering the perspective of ones own candidate compared with the opponent, and this effect was amplified closer to the election. Taken together, these results highlight ways in which ability and motivational relevance modulate socio-affective processing of the attitudes of others.

Mirroring, Mentalizing, and the Social Neuroscience of Listening

Listening to another speak is a basic process in social cognition. In the social neurosciences, there are relatively few studies that directly bear on listening; however, numerous studies have investigated the neural bases of some of the likely constituents of successful listening. In this article, I review some of this work as it relates to listening, with a focus on two auxiliary processes in the comprehension of speech: perceiving the nonverbal behaviors, such as facial expression, that accompany an utterance (i.e., how it is being said); and interpreting an utterance and the nonverbal behaviors that accompany it in terms of the speakers state of mind (i.e., why it is being said). The review indicates the presence of two large-scale systems in the human brain that play a major role in successful listening: the putative mirror neuron system, which likely facilitates the relatively automatic perception of the how of speech; and the so-called mentalizing system, which likely underlies our ability to actively reach conclusions about the why of speech behavior. I conclude by considering the possibility that the dynamic interaction of mirroring and mentalizing processes may be pivotal for successful listening and social interaction more generally.