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Atypical Frontal-Posterior Synchronization of Theory of Mind Regions in Autism During Mental State Attribution

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Atypical Frontal-Posterior Synchronization of Theory of Mind Regions in Autism During Mental State Attribution SOCIAL NEUROSCIENCE, 2009, 4 (2), 135Á152 Atypical frontal-posterior synchronization of Theory of Mind regions in autism during mental state attribution Rajesh K. Kana Carnegie Mellon University, Pittsburgh, PA, USA, and University of Alabama, Birmingham, AL, USA Timothy A. Keller and Vladimir L. Cherkassky Carnegie Mellon University, Pittsburgh, PA, USA Nancy J. Minshew University of Pittsburgh School of Medicine, Pittsburgh, PA, USA Marcel Adam Just Carnegie Mellon University, Pittsburgh, PA, USA This study used fMRI to investigate the functioning of the Theory of Mind (ToM) cortical network in autism during the viewing of animations that in some conditions entailed the attribution of a mental state to animated geometric figures. At the cortical level, mentalizing (attribution of metal states) is underpinned by the coordination and integration of the components of the ToM network, which include the medial frontal gyrus, the anterior paracingulate, and the right temporoparietal junction. The pivotal new finding was a functional underconnectivity (a lower degree of synchronization) in autism, especially in the connections between frontal and posterior areas during the attribution of mental states. In addition, the frontal ToM regions activated less in participants with autism relative to control participants. In the autism group, an independent psychometric assessment of ToM ability and the activation in the right temporoparietal junction were reliably correlated. The results together provide new evidence for the biological basis of atypical processing of ToM in autism, implicating the underconnectivity between frontal regions and more posterior areas. Keywords: Autism, Mentalizing, Theory of Mind (ToM), Mental state, fMRI, Underconnectivity. INTRODUCTION 1985; Baron-Cohen, Campbell, Karmiloff-Smith, Grant, & Walker, 1995; Leekam & Perner, 1991; Even though difficulty with Theory of Mind (ToM) Perner, Frith, Leslie, & Leekam, 1989; Reed & processing in autism has been demonstrated in Peterson, 1990; Swettenham, 1996; Swettenham, many studies (e.g., Baron-Cohen, Leslie, & Frith, Baron-Cohen, Gomez, & Walsh, 1996), only a few Correspondence should be addressed to: Rajesh K. Kana, Department of Psychology, University of Alabama, Birmingham, AL 35294, USA. E-mail: [email protected] This research was supported by Collaborative Program of Excellence in Autism (CPEA) Grant HD35469 from the National Institute of Child Health and Human Development and the Cure Autism Now Young Investigator Award to Rajesh K. Kana. The authors thank Fulvia Castelli (King’s College, London, UK) for generously providing the animation stimuli for our study. The authors also thank Diane Williams for her assistance in collecting the ToM scores, Sarah Schipul and Stacey Becker for assistance with the data collection and data analysis, and Rachel Krishnaswami for editorial comments on an earlier version of the manuscript. # 2009 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business www.psypress.com/socialneuroscience DOI:10.1080/17470910802198510 136 KANA ET AL. neuroimaging studies have explored this domain in clear in showing that human thought involves a autism (e.g. Happe et al., 1996; Castelli, Frith, network of cortical areas whose activity is co- Happe´, & Frith, 2002; see Frith, 2001 for a review). ordinated (synchronized), and that coordination The impairment in ToM (processing the mental has to be based on interregional communication, states of others) in autism often results in difficul- using the white matter tracts that provide the ties with the communications and interactions that anatomical connectivity. The functional magnetic underpin everyday life. Attributing mental states resonance imaging (fMRI) findings emerging in (or mentalizing) is perhaps one of the most the past few years indicate that the synchroniza- complex forms of reasoning in which humans tion between frontal and posterior areas is lower engage. It involves the interplay of a set of in autism (Just et al., 2004; Just et al., 2007; Kana, subprocesses, such as representation of reality, Keller, Cherkassky, Minshew, & Just, 2006; understanding one’s own beliefs and the beliefs Koshino et al., 2005; Villalobos, Mizuno, Dahl, of others, and decoupling beliefs from reality. Kemmotsu, & Muller, 2005). For example, in a Disruption of such complex information proces- Tower of London (TOL) problem-solving task, sing is a fundamental impairment in people with which entails activation of both frontal and autism (Minshew, Goldstein, & Siegel, 1997). At parietal areas, the synchronization between the the cortical level, such complex information-pro- frontal and parietal areas is lower in autism than cessing requires the integration of the activity of in a control group. multiple brain regions. According to the under- Neuroimaging studies of ToM processing have connectivity theory of autism (Just, Cherkassky, identified a frontal-posterior network of brain Keller, Kana, & Minshew, 2007), whenever inter- regions that include the medial prefrontal cortex, region connectivity and coordination come into the temporal-parietal junction at the top of the play, an underconnected system can manifest superior temporal sulcus, and the temporal poles impairments, particularly when there is a large adjacent to the amygdala (Brunet, Sarfati, Hardy- load on the system. ToM processing is supported by Bayle, & Decety, 2000; Castelli, Frith, Happe´,& a network of several discrete neural structures that Frith, 2000; Castelli, Happe´, Frith, & Frith, 2002; require connectivity among themselves to provide Fletcher et al., 1995; Gallagher et al., 2000; the integrated functioning. The purpose of the Vogeley et al., 2001). There has been some debate study reported here was to establish whether the concerning the differential roles of frontal versus differences in ToM processing in autism are related posterior regions in ToM processing. Although to a disruption of processing at the cortical network the study reported below does not focus on level and not just at the level of individual cortical differentiating the contributions of various brain areas. areas to ToM processing, it is nevertheless useful The previously proposed theory of cortical to acknowledge that different areas are very underconnectivity (Just, Cherkassky, Keller, & likely playing different roles. Some researchers Minshew, 2004) starts with the propositions that argue that while the medial frontal cortex is interregional connective circuitry in the brain is directly involved in mental state reasoning and disrupted in autism, and that patterns of thought decisions, the right temporoparietal junction col- that are particularly dependent on integration of lates the cues that are the input to mentalizing frontal and more posterior contributions are (Gallagher & Frith, 2003). Others argue that the disrupted (Just et al., 2007). Furthermore, the right temporoparietal junction is the central theory attributes ToM deficits and executive player in mental state reasoning, not only collat- function disruption to such underconnectivity. It ing but also processing the cues to compute a proposes a causal link between the anatomical, mental state (Saxe & Kanwisher, 2003). Regard- physiological (brain activity), and psychological less of the precise computation that each area phenomena. Specifically, the theory posits that performs in ToM processing, it appears that the the communication bandwidth among cortical two regions function in concert with each other. It areas, particularly between frontal and posterior is this coordination among the contributing areas areas, is lower in autism than in typical partici- that is the focus of this article. pants. Bandwidth, which refers here to the The communications with the frontal compo- amount of information that can be transmitted nents of the ToM network are of special interest between cortical centers per unit time, is a critical here, because of the hypothesis of lower frontal- factor in the performance of a computational posterior functional connectivity in autism. A network. Brain imaging research has been very number of studies indicate that the role of frontal THEORY OF MIND NETWORK IN AUTISM 137 lobe regions in processing ToM is major. Evi- such as medial frontal cortex and right tempor- dence for this view comes in large part from oparietal junction. This hypothesis is based on the lesion research. Patients with damage to frontal findings from studies of impairment in ToM cortex are frequently impaired in the perfor- (Castelli et al., 2002), and perception of biological mance of ToM tasks (Stuss, Gallup, & Alexander, motion (Blake, Turner, Smoski, Pozdol, & Stone, 2001). Damage to the anterior prefrontal regions 2003) in autism. The novel portion is our predic- has been associated with impaired self-awareness tion of functional underconnectivity in autism for the appropriateness of social interactions, during mentalizing, especially in connections judgment and planning difficulties (Stuss, 1991), involving the frontal lobe. This prediction is based as well as impaired awareness of the mental states on previous findings of functional underconnec- of others (Stone, Baron-Cohen, & Knight, 1998; tivity in autism in a wide variety of higher Stuss et al., 2001). cognitive tasks in autism (Just et al., 2007; Kana It may not be just the frontal activation that is et al., 2006; Castelli et al., 2002). The under- critical; the synchronization of frontal activity connectivity prediction is also
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