Ji-Won Hur1, Randolph Blake2, Kang Ik K Cho3, Jejoong Kim4, So-Yeon Kim4, Soo-Hee Choi5, Do-Hyung Kang5, Jun Soo Kwon6. 1. Department of Brain and Cognitive Sciences, Seoul National University, Seoul, Republic of Korea2Department of Psychology, Chung-Ang University, Seoul, Republic of Korea. 2. Department of Brain and Cognitive Sciences, Seoul National University, Seoul, Republic of Korea3Department of Psychology, Vanderbilt University, Nashville, Tennessee. 3. Department of Brain and Cognitive Sciences, Seoul National University, Seoul, Republic of Korea. 4. Department of Psychology, Duksung Women's University, Seoul, Republic of Korea. 5. Department of Psychiatry, Seoul National University College of Medicine, Seoul, Republic of Korea. 6. Department of Brain and Cognitive Sciences, Seoul National University, Seoul, Republic of Korea5Department of Psychiatry, Seoul National University College of Medicine, Seoul, Republic of Korea.
Abstract
IMPORTANCE: Exploration of the ability to process socially relevant events portrayed by biological motion and to identify underlying neuronal processes can provide clues for understanding the pathophysiology of psychosis. Individuals with schizotypal personality disorder (SPD) have pervasive interpersonal deficits and odd behaviors. An understanding of the neural mechanisms involved in the perception of biological motion and the relation of activity to clinical symptoms in those mechanisms is needed. OBJECTIVE: To investigate the specificity of brain regions responsive to biological motion perception in individuals with SPD compared with healthy control individuals. DESIGN, SETTING, AND PARTICIPANTS: Twenty-one patients diagnosed as having SPD and 38 age-, sex-, and IQ-matched controls underwent event-related functional magnetic resonance imaging. The SPD group completed the Scale for the Assessment of Positive Symptoms, the Scale for the Assessment of Negative Symptoms, and the Schizotypal Personality Questionnaire for assessment of symptom severity. During scanning, all participants were required to discriminate biological from scrambled sequences of point-light animations. Data were collected from September 21. 2011, to July 13, 2013, and analyzed from March to May 2015. MAIN OUTCOMES AND MEASURES: Blood oxygenation level-dependent signals during event-related scanning and symptom severity in the SPD group. RESULTS: The 21 individuals with SPD (16 men and 5 women) and 38 controls (29 men and 9 women) had a mean (SD) age, 22.8 (3.8) vs 22.2 (2.5) years and a mean (SD) IQ, 115.00 (12.55) vs 120.24 )7.68). Brain imaging revealed the presence of neuronal activation specific to biological motion within the posterior superior temporal sulcus. However, the individuals with SPD exhibited regions of neural responsiveness within brain regions forming the reward network, which consisted of the dorsal striatum and bilateral superior medial frontal cortex (all t ≥ 2.99, P of clusters <.002). The individuals with SPD also exhibited reduced activation in the anterior and middle cingulate cortices and the lingual and superior occipital gyri, which are brain areas responsive to biological motion perception and executive control of perception (all t ≥ 3.29, P of clusters <.001). In addition, significant correlations between the hyperdopaminergic clinical symptoms and enhanced neuronal activation in the caudate nucleus and frontal cortex were observed in the SPD group (all r ≥ 0.52, P < .02). CONCLUSIONS AND RELEVANCE: Individuals with SPD display heightened activation in the neural circuitry involved in reward and decision making when viewing biological motion stimuli in addition to a positive correlation between increased blood oxygenation level-dependent signal responses related to biological motions and clinical symptoms. These findings suggest that enhanced responses arise within the reward network in individuals with SPD and are possibly related to the peculiar ways that individuals with SPD behave in social contexts.
IMPORTANCE: Exploration of the ability to process socially relevant events portrayed by biological motion and to identify underlying neuronal processes can provide clues for understanding the pathophysiology of psychosis. Individuals with schizotypal personality disorder (SPD) have pervasive interpersonal deficits and odd behaviors. An understanding of the neural mechanisms involved in the perception of biological motion and the relation of activity to clinical symptoms in those mechanisms is needed. OBJECTIVE: To investigate the specificity of brain regions responsive to biological motion perception in individuals with SPD compared with healthy control individuals. DESIGN, SETTING, AND PARTICIPANTS: Twenty-one patients diagnosed as having SPD and 38 age-, sex-, and IQ-matched controls underwent event-related functional magnetic resonance imaging. The SPD group completed the Scale for the Assessment of Positive Symptoms, the Scale for the Assessment of Negative Symptoms, and the Schizotypal Personality Questionnaire for assessment of symptom severity. During scanning, all participants were required to discriminate biological from scrambled sequences of point-light animations. Data were collected from September 21. 2011, to July 13, 2013, and analyzed from March to May 2015. MAIN OUTCOMES AND MEASURES: Blood oxygenation level-dependent signals during event-related scanning and symptom severity in the SPD group. RESULTS: The 21 individuals with SPD (16 men and 5 women) and 38 controls (29 men and 9 women) had a mean (SD) age, 22.8 (3.8) vs 22.2 (2.5) years and a mean (SD) IQ, 115.00 (12.55) vs 120.24 )7.68). Brain imaging revealed the presence of neuronal activation specific to biological motion within the posterior superior temporal sulcus. However, the individuals with SPD exhibited regions of neural responsiveness within brain regions forming the reward network, which consisted of the dorsal striatum and bilateral superior medial frontal cortex (all t ≥ 2.99, P of clusters <.002). The individuals with SPD also exhibited reduced activation in the anterior and middle cingulate cortices and the lingual and superior occipital gyri, which are brain areas responsive to biological motion perception and executive control of perception (all t ≥ 3.29, P of clusters <.001). In addition, significant correlations between the hyperdopaminergic clinical symptoms and enhanced neuronal activation in the caudate nucleus and frontal cortex were observed in the SPD group (all r ≥ 0.52, P < .02). CONCLUSIONS AND RELEVANCE: Individuals with SPD display heightened activation in the neural circuitry involved in reward and decision making when viewing biological motion stimuli in addition to a positive correlation between increased blood oxygenation level-dependent signal responses related to biological motions and clinical symptoms. These findings suggest that enhanced responses arise within the reward network in individuals with SPD and are possibly related to the peculiar ways that individuals with SPD behave in social contexts.
Authors: Anna R Docherty; Andrey A Shabalin; Daniel E Adkins; Frank Mann; Robert F Krueger; Silviu-Alin Bacanu; Archie Campbell; Caroline Hayward; David J Porteous; Andrew M McIntosh; Kenneth S Kendler Journal: Schizophr Bull Date: 2020-03-27 Impact factor: 9.306