Social interaction and communication begin in early infancy, and, although these are fundamental human functions, little is known about the underlying neural mechanisms that regulate them particularly in Autism Spectrum Disorder (ASD). ASD is a neurodevelopmental disorder characterized by significant disabilities in language and social skills, and the specific neural mechanisms that lead to these disabilities remain active topics for investigation. Emerging theoretical directions converge on problems with eye-contact as a salient component of these communication and social disabilities. Technical limitations, however, associated with imaging of two or more individuals during natural communication and mutual eye contact have been a primary obstacle to these investigations. To overcome this technical impasse, we employ a rapidly developing brain imaging technology, functional near-infrared spectroscopy (fNIRS) allowing simultaneous neural imaging of two individuals during valid interactions to observe the neural effects of eye-to-eye contact and actual dialogue. Functional NIRS detects active neural tissue based on the blood-oxygen-level-dependent (BOLD) signal by measuring variations in the absorption spectra associated with oxyhemoglobin and deoxyhemoglobin. Because detectors and emitters are surface mounted on the head, they are relatively insensitive to head movement, and, as such, fNIRS is well suited for investigations of neural events engaged during active interpersonal interactions between two participants. The neural mechanisms that underlie atypical interpersonal interactions and eye contact in adult ASD are the focus of this proposal. Pilot studies confirm the feasibility of all aspects of this research project. Dyads consisting of a confederate and a participants with typical development (TYP) or ASD will be compared during neuroimaging while engaged in natural interaction and communication. We introduce a computational approach based on wavelet analysis to quantify regional cross-brain coherence between the two participants and hypothesize that cross-brain coherence associated with speech and eye contact will be reduced in ASD relative to the TYP cohort. Cross-brain computations also form the basis for a model of dynamic neural processes based on neural ?send and receive? functions during communication. We hypothesize that these dynamic ?cross-brain communication? systems unify and coordinate the roles of language production and reception (Broca's and Wernicke's Areas), respectively, with visual reception involving face specializations (fusiform gyrus). Computational comparison of cross-brain connectivity effects as well as conventional functional connectivity and segregation/contrast effects during live communication both with and without direct eye contact provides a transformational technical, empirical, computational, and theoretical advance toward understanding the dynamic neural mechanisms associated with social and communication disabilities in ASD.

Public Health Relevance

Although deficits in language skills, social communication, and eye contact are core features of autism spectrum disorder (ASD), the underlying neural mechanisms are only partially understood, primarily due to the absence of techniques that enable direct observations of two individuals during ecologically valid interactions. This study pioneers a novel approach to image neural activity acquired simultaneously during interpersonal interactions between two adults using recent advances in functional near-infrared spectroscopy, fNIRS, a minimal risk neuroimaging technique that acquires blood oxygen-level dependent, BOLD, signals with head-mounted optodes rather than an MRI scanner. Using this novel two-brain paradigm, we aim to compare the neural effects of real eye-to-eye contact and real interpersonal dialogue for typical adults (TYP) and adults with ASD to advance our understanding of the neural mechanisms that underlie deficits in real-time dynamic social interactions and communication.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
5R01MH111629-04
Application #
9726068
Study Section
Child Psychopathology and Developmental Disabilities Study Section (CPDD)
Program Officer
Gilotty, Lisa
Project Start
2016-09-26
Project End
2021-06-30
Budget Start
2019-07-01
Budget End
2020-06-30
Support Year
4
Fiscal Year
2019
Total Cost
Indirect Cost
Name
Yale University
Department
Psychiatry
Type
Schools of Medicine
DUNS #
043207562
City
New Haven
State
CT
Country
United States
Zip Code
06520
Dravida, Swethasri; Noah, Jack Adam; Zhang, Xian et al. (2018) Comparison of oxyhemoglobin and deoxyhemoglobin signal reliability with and without global mean removal for digit manipulation motor tasks. Neurophotonics 5:011006
Pinti, Paola; Tachtsidis, Ilias; Hamilton, Antonia et al. (2018) The present and future use of functional near-infrared spectroscopy (fNIRS) for cognitive neuroscience. Ann N Y Acad Sci :
Rolison, Max J; Naples, Adam J; Rutherford, Helena J V et al. (2018) Modulation of reward in a live social context as revealed through interactive social neuroscience. Soc Neurosci 13:416-428
Rojiani, Rahil; Zhang, Xian; Noah, Adam et al. (2018) Communication of emotion via drumming: dual-brain imaging with functional near-infrared spectroscopy. Soc Cogn Affect Neurosci 13:1047-1057
Piva, Matthew; Zhang, Xian; Noah, J Adam et al. (2017) Distributed Neural Activity Patterns during Human-to-Human Competition. Front Hum Neurosci 11:571
Noah, J Adam; Dravida, Swethasri; Zhang, Xian et al. (2017) Neural correlates of conflict between gestures and words: A domain-specific role for a temporal-parietal complex. PLoS One 12:e0173525
Lapborisuth, Pawan; Zhang, Xian; Noah, Adam et al. (2017) Neurofeedback-based functional near-infrared spectroscopy upregulates motor cortex activity in imagined motor tasks. Neurophotonics 4:021107
Zhang, Xian; Noah, Jack Adam; Dravida, Swethasri et al. (2017) Signal processing of functional NIRS data acquired during overt speaking. Neurophotonics 4:041409
McPartland, James C (2017) Developing Clinically Practicable Biomarkers for Autism Spectrum Disorder. J Autism Dev Disord 47:2935-2937
Hirsch, Joy; Zhang, Xian; Noah, J Adam et al. (2017) Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact. Neuroimage 157:314-330