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R Lajiness-O'Neill 1,2 , AM Chase 1 , A Olszewski 1 , MA Boyle 1 ,

Hemispheric Differences in Neural Activation During Gaze Cueing in Autism Spectrum Disorder (ASD) Measured by Magnetoencephalography (MEG). R Lajiness-O'Neill 1,2 , AM Chase 1 , A Olszewski 1 , MA Boyle 1 , L Pawluk 1 , A Mansour 1 , D Jacobson 1 , ML Gallaway 1 ,

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R Lajiness-O'Neill 1,2 , AM Chase 1 , A Olszewski 1 , MA Boyle 1 ,

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  1. Hemispheric Differences in Neural Activation During Gaze Cueing in Autism Spectrum Disorder (ASD) Measured by Magnetoencephalography (MEG) R Lajiness-O'Neill1,2, AM Chase1, A Olszewski1, MA Boyle1, L Pawluk1, A Mansour1, D Jacobson1, ML Gallaway1, P Lewandowski-Powley1, B. Gorka1, J Moran2, and SM Bowyer2,3,4 1Eastern Michigan University, Ypsilanti, MI, USA 2 Henry Ford Hospital, Detroit, MI, USA; 3Wayne State University, Detroit, MI, USA; 4Oakland University, Rochester, MI USA

  2. Social Cognition What is and why are we interested in social cognition? What are the theories that guide our investigations? Adolphs (2003) Theory of Mind (Baron-Cohen, Leslie, & Frith, 1985) Integrative, heuristic model of social competence by Yeates et al. (2007) Can we define the “critical” brain regions, neural networks, social variables? STS, inferior temporal (fusiform), medial and orbitofrontal, inferior parietal MNS Gaze cueing/joint attention Affect recognition, facial recognition Can we adequately operationalize important terms in social cognition? Competence? Can we measure these constructs in valid and reliable ways? Outcome? Which is the SIP (social information processing) variable and which is outcome variable? Empathy? Can we remediate these skills?

  3. What is Social Cognition? Not just social Not just language – although does significantly impact regulation of social behavior Emotion – appears to tightly linked to social functioning Moral behaviors Brain regions linked to emotional processing are also important for social functioning A common ancestor about 6m years ago, and their DNA remains highly similar - between 96% and 99% identical Genetic differences between a human and a chimp are however 10 times more than between any two humans

  4. Why Should We Be Interested in Social Cognition? “We are intensely social species – it has been argued that our social nature defines what makes us human, what makes us conscious or what gives us our large brains.” (Adolphs, 2003) Field of social neuroscience and social cognition has emerged from a converging of the areas of sociobiology/evolutionary and social psychology. Neuropsychology, neuroscience, developmental Both innate/cognitive and acquired/contextual aspects of behavior

  5. Course Perceptual • Processing • Superior Colliculus • Detailed Perceptual • Processing • Fusiform Gyrus • Superior Temporal Gyrus • Motivational Evaluation • Amygdala • Orbitofrontal Cortex • Ventral Striatum • Representation of • Perceived Action • Left Frontal Operculum • Superior Temporal Gyrus Reappraisal Self- regulation • Emotional Response • in Body • Visceral, autonomic, • endocrine changes • Modulation of Cognition • Cingulate Cortex • Hippocampus • Basal Forebrain • Representation of • Emotional Response • Somatosensory-related • Cortices • Social Reasoning • Prefrontal Cortex (Adapted from Nature Reviews/Neuroscience, Adolphs, 2003)

  6. Critical Role of Eyes and Gaze in Face ProcessingSpend more time on internal features (eyes, nose, mouth) than external features.Carry information necessary for emotion recognition thus critical for non-verbal communicationScanning always starts with eyes despite emotion.(Jones, Klin, & Carr 2008)

  7. Orienting of Attention by Gaze and Gaze Perception Amygdala, STG/STS, ventro-temporal regions (e.g., fusiform), parietal, and frontal regions suggest and frontoparietal circuit for gaze (Meta-analysis by Grosbras et al., 2005) Superior temporal sulcus (STS) and gyrus (STG) activate when subjects view stimuli depicting biological motion and mouth movements Basic gaze cueing paradigms using schematic drawings or real life photographs (Frischen, Bayliss, & Tipper, 2007; Itier & Batty, 2009; Martinez & Benavente, 1998)

  8. We understand other people’s behavior, in part, by simulation—putting ourselves in their shoes. Mirror Neuron System (MNS) – imitating another’s action through observation activates the premotor cortex and it is somatotopic with respect to body part (should correlate with empathy, social IQ) Premotor and parietal cells in macaque brain Plausible neurophysiological mechanism for complex social behaviors, from imitation to empathy(Iacoboni & Dapretto, 2006)

  9. Motoric description of action Inferior Parietal Lobule Goal of action Frontoparietal Mirror Neuron System Inferior Frontal Ventral Premotor Posterior STS Efferent copies of motor imitative commands to allow match between sensory predictions of imitative motor commands and visual description of observed action Mirror neuron properties Main visual input

  10. Imitative behavior is critical for social cognitive functions Chameleon effect – we imitate each other automatically when interacting socially The more people imitate the more they tend to be empathic MNS insula limbic system ---- could provide ability to empathize through representation and “inner imitation” of actions of others MNS also believed to be important in encoding other’s intentions (Iacoboni et al., 2005)

  11. An Integrative Model of Social Competence (Yeates, et. al., 2007)

  12. Social dysfunction is a pervasive component of many developmental and acquired disorders and is evident in most psychopathologies. Social competence is a strong predictor of outcome in these and other disorders. (Rubin, Bukowksi, & Parker, 2006) Autism Spectrum Disorders Depression/Anxiety Schizophrenia Personality Disorders Traumatic Brain Injury What are critical endophenotypic markers? Joint Attention? Which cognitive and behavioral features should we focus on?

  13. Autism Spectrum Disorders (ASD) Autism Spectrum Disorders (ASD) – a Social Communication Disorder Deficits in communication and social functioning coupled with rigid, inflexible behaviors and interests.

  14. A Growing Problem – Prevalence & Economics Centers for Disease Control (CDC) Center for Disease Control and Prevention (MMWR Surveillance Summary, 2007) - prevalence at ≈ 1 in 150 Current CDC reported ASD prevalence is 1 in 110, making its etiology and early identification an urgent public health concern $50,000 Cost per child per year for 1 therapy Applied Behavior Analysis $3,000,000 Lifetime cost for dependent individual $35-90 billion annual societal cost Higher number comparable to cost of Alzheimer’s disease (Ganz, 2007; Jarbrink & Knapp, 2001)

  15. Joint attention (JA) - refers to behaviors that allow an individual to communicate nonverbally through eye gaze/gesture. JA is an important precursor to language (Morales et al., 2000) and related to positive social behaviors in children (Sheinkopf et al., 2004).

  16. Neurotypicals Developmental Research shows Joint Attention (14 M) & Pretend Play (18-24M) evident early in life.

  17. Gaze Cueing Joint Attention Has been postulated to be critical in helping others to make mentalistic inferences that guide behavior from viewing expressions in the eyes. Joint attention has been found to be an important precursor to language development. Infant response to joint attention (RJA) related to positive social behaviors in preschool at-risk children. Joint Attention – in neurotypicals purported to require integrity of superior temporal sulcus (STS), superior temporal gyrus, and adjacent cortex on the surface of the angular gyrus and ventromedial frontal regions.

  18. Reversed asymmetry of language suggests displacement of regions that underlie facial processing, eye-gaze cueing, and joint attention and aberrant frontoparietal and frontotemporal connectivity that may partially underlie social dysfunction in autism. (Flagg, Cardy, Roberts, Roberts, 2005; Redcay, 2008)

  19. Current Study • Our hypothesis - “Crowding” in regions that underlie both social and speech perception in the right inferior parietal and superior temporal lobes (e.g. IP and STS) due to altered hemispheric specialization. • Contextual differences based on stimuli attended to in individuals with ASD compared to neurotypicals • Words and faces chosen given hypervigilance to orthographs seen in ASD compared to difficulty attending to faces of others.

  20. Methods • Participants • Six ASD Ss (Mean Age – 16.6; Mean IQ – 120 • Eight Neurotypicals (Mean Age – 17.5; Mean IQ - 115) • Autism Diagnostic Interview-Revised (ADI-R) confirmed diagnosis

  21. Magnetoencephalography • Individuals viewed a digital photograph of a character whose gaze was shifted toward or away from (congruent vs. incongruent) targets (asterisk), printed words, or faces projected onto a screen. • The subject was asked to press the button when the subject was looking toward something. • 148 channel whole head MEG (4D Neuroimaging, Magnes WH2500) collected cortical activity. Evoked magnetic field data was used from -0.2 seconds prior until 0.65 seconds after the stimulus onset. Brain activity was analyzed with MR-FOCUSS, a current density technique.

  22. Magnetoencephalography • Latency of onset • Normalized Amplitudes – average normalized amplitude per active sources in 54 brain regions based on MNI coordinates was calculated for each subject. • The left and right hemisphere ROI’s were summed and averaged based on total active sources for the ROI to generate a normalized mean amplitude for the ROI over the 650 ms epoch to compare groups. • Differences examined with t-statistic. • p-values were not corrected for multiple comparisons due to the small N. Significance p<.05

  23. PAPER

  24. Results Gaze Cues Targets • Significant differences in normalized mean amplitudes in ASD compared to controls with higher amplitudes in ASD in Left posterior cortical regions whereas Controls displayed higher amps in Right inferior temporal and middle orbitofrontal regions • No differences in onset of activation

  25. Gaze Cues to Target (Asterisk) Condition - Amplitudes

  26. Results Gaze Cues Words • Significantly higher normalized mean amplitudes in left superior occipital region in ASD and right putamen in controls. • Recent pathway through Putamen has been postulated that might connect the ventral anterior occipito-temporal sulcus (aOT) to articulatory areas in the precentral cortex (PrC). (Seghier & Price, 2010) • Latency – Earlier onset in middle frontal and superior frontal and supramarginal regions in controls (≈200ms) compared to ASD (≈350ms).

  27. Gaze Cues to Words Condition - Amplitudes

  28. Gaze Cues to Words Condition - Latency

  29. In ASD activation occurring throughout the epoch – my reflect hypervigilance to words and extended recruitment by these regions, limiting the frontal regions ability to activate for social cues.

  30. Results Gaze Cues Faces • Significantly higher mean amplitudes in left angular in ASD. Left angular regions critical in word reading in neurotypicals. Activation occurring at ≈200 ms. • At this same latency, neurotypicals activating right frontoparietal regions. • Significantly earlier onset in ASD (≈200ms) in inferior temporal regions than in controls (≈300ms). • Double dissociation - Controls displayed earlier onset to words in frontal regions and later to faces in temporal regions while ASD had earlier onset to faces in temporal regions and later onset to words in frontal regions.

  31. Gaze Cues to Faces Condition - Amplitudes

  32. Gaze Cues to Face A B Right frontoparietal activation in control subject (A) at 194 ms (above) while ASD subject (B) has significant activation in left parietal regions during face condition at 194 ms (below).

  33. Gaze Cues to Faces Condition - Latency

  34. Summary • The neurobiological underpinnings of gaze cueing in children and adolescents with ASD are poorly understood and could have significant implications for understanding the etiology of social impairment. • Joint attention is likely an important endophenotypic variable. • Results of this study revealed higher mean amplitudes in left occipital and parietal brain regions during gaze shifts to both targets and faces in ASD. • Findings are consistent with recent ERP study which demonstrated stronger parietal responses in children with ASD during face processing and could reflect a compensatory analytical strategy to process facial information (Wong et al., 2008). • In contrast, higher mean amplitudes in right inferior temporal and medial orbitofrontal regions was evident in controls, the latter of which has been implicated in the social cognitive network. • Pronounced left angular amplitudes were also noted in left parietal, specifically angular, regions during gaze shifts to faces in ASD.

  35. Conclusions • ASD subjects appear to be using regions that underlie skills necessary for reading, including posterior parietal and occipital regions for joint attention to gaze shifts. • This may be due to “crowding” or altered hemispheric specialization in regions that underlie both social and speech perception, such as the right inferior parietal and superior temporal lobe (e.g. IP and STS). • We believe the crowding occurs not only due to competition in regions that underlie social and “speech” perception, but both oral and written “language” perception in general.

  36. Henry Ford Health System Dr. Susan Bowyer Dr. John Moran Funding New Faculty Award Faculty Research Fellowship Eastern Michigan University Eastern Michigan University Lesley Pawluk Daniel Jacobson Amy Olszewski Kelly Luce Dr. Alfred Mansour Adam Chase Mellisa Boyle Michelle Gallaway Bethany Gorka Paula Lewandowski-Powley Aimee Moore Natalie Morris Larry Kowalski Acknowledgments

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