Effects of Coordination Exercises on Social Functioning: Evidence from fMRI and Social - ability Measures

Objective : Research has demonstrated the positive effects of physical activities on social cognition. The purpose of the present study was to find out whether coordination exercises have a beneficial effect on enhancing social functioning. We investigated the activation of the brain areas associated with doing one-person coordination exercises, as compared to doing two-person coordination exercises. We were interested in testing the hypothesis that two-person coordination exercises activate those brain areas underlying communication abilities, empathy in“theory of mind”(ToM), and working memory in social cognition. Materials : Thirty-four Japanese college students served as subjects. Methods : In the MRI system, the subjects carried out block-designed cognitive tasks containing affective visual stimuli (pleasant, unpleasant, and neutral stimuli). Then they got out of the MRI system and performed both one-person coordination and two-person coordination exercises. Just after the exercises, they were retested using the same types of the affective stimuli in the MRI system. We examined social abilities in terms of empathizing and memory span. Results : The present study provided evidence that coordination exercises activate language, working memory, and theory of mind functions. One of the fMRI results to be noted is that the right, but not the left, anterior cingulate correlated with the working memory function. Conclusions : We provided evidence for the effect of performing coordination exercises on the activation of the left frontal gyrus related to social functioning. We could also provide support for the hypothesis that two-person coordination exercises activate both the working memory function and the ToM function.


Introduction
The effect of physical activity has been shown not only on motor performance but also cognitive performance. Prior research has shown a positive correlation between physical activity and cognitive performance in older adults 1) 2) . Some studies have suggested, especially from the viewpoints of hippocampal neurogenesis and neural plasticity, that physical activity improves brain functions and prevents decline of cognition 3) 4) . Furthermore, several studies, especially from the viewpoints of social functioning and brain functions, showed that physical exercise is a significant factor in academic performance 5) . A large population-based study demonstrated that physical exercise can be an important instrument for optimizing not only academic achievements but also social cognition 6) .
Regarding interrelationships between physical exercise and social functioning, common higher brain function has attracted a great deal of attention 7) . Major components of social communication, working memory, and social cognition play a decisive role in social functioning. The"theory of mind (ToM) advocated by  ; the ability to understand, predict, and empathize othersʼ feelings and intensions; is a crucial functioning in social cognition. ToM-related neuroimaging and lesion studies found ToM-related activity in the medial prefrontal cortex 9) . Mochizuki, Sudo, Kirino, and Itoh 10) examined the brain activation associated with motor imagery of coordination exercises and social abilities, and tested the hypothesis that viewing one-person coordination exercises vs. twoperson coordination exercises contributes to different degrees of brain activation. The coordination exercises are the ones which improve coordination abilities. Coordination abilities can be defined as the integrated abilities of muscles and neurons 11) . The result of the above-mentioned study 10) suggested the importance of having a partner, rather than the use of tools, and further indicated ToM-related effects in exercises. The studies on empathy, a factor in social cognition, reported some specific brain areas such as left and right insula, inferior frontal gyrus and parts of the cingulate cortex 12) .
As noted in the above review, research has confirmed effects of physical activity on brain activation. Most of the studies dealt with the effect of cardiovascular exercise on cognitive performance. However, the influence of other types of exercise has not been well investigated. A series of studies on the effect of coordination exercise on brain activities reported interrelationships among coordination exercise, social cognition, language proficiency, and brain activation 10) 13)-15) . Mochizuki et al. 10) investigated brain activation of specific areas related to viewing coordination exercises and suggested that exercises done by two persons require more sophisticated communication than those done by one person. Recent research has reported that coordination training facilitates brain function and cognitive performance 16) . Coordinative exercises and motor coordination are reported to be related to cognitive function, including executive functions. Budde et al. 17) verified that 10 minutes of acute bilateral coordination exercises promoted more improvement in concentration and attention of school children than a normal physical education lesson with the same duration. Fernandes et al. 18) indicated that visual motor coordination and visual selective attention may influence academic achievement and cognitive function. Regarding movement therapy, research suggests a beneficial effect of movement therapy on enhanced physical, mental, and emotional functioning 19) . We are interested in investigating a possibility of the use of coordination exercises as one type of movement therapy for enhancing cognitive functioning as well as physical functioning.
The purpose of the present study was to find out whether coordination exercises have a beneficial effect on enhancing social functioning. Among the features of coordination exercises, we attempted to study the effect of doing two-person coordination exercises on social functioning, as compared to doing one-person coordination exercises. We attempted to test the hypothesis that doing twoperson coordination exercises evokes those brain areas underlying social functioning which include communication abilities, empathy, ToM and working memory in social cognition. In this study, ToM is interpreted as a social perceptual and predictive ability related to cognitive empathy 20) .
Concretely, we designed the experiment on affective control, which measured the differences in the cognition of affective stimuli before and after doing two-person coordination exercises, as compared to one-person coordination exercises. We used a within-subject design.

Participants and Methods
There were three sessions in the present study: the fMRI session, the coordination exercise session, and the social ability session. We held these three sessions on the same day for each subject. The design of the fMRI session and the coordination exercise session for each subject is shown in  followed the above-mentioned two sessions.

Participants
Thirty-four healthy college students (19 males and 15 females, 21.2 ± 1.2 years old) served as subjects. They were all Japanese undergraduate students who belonged to a school of health and sports science. The study protocol, which was in accordance with the Declaration of Helsinki, was approved by the Ethics Committees of Juntendo Shizuoka Hospital (#RIN-466). After a complete description of the study was given to all subjects, they gave informed consent for the protocol.

Social ability session
In this study, we examined social abilities in terms of two specific components: empathizing and memory span. These personal social abilities are generally assessed by self-report questionnaires as convenient but effective measures derived from structured interviews such as the Structured Clinical Interview (DSM-V). There are many simple self-report scales available to measure individual ability to recognize otherʼs emotions and mental states. A set of self-reports were administered including Systemizing Quotient (SQ), Empathy Quotient (EQ), and Autism Spectrum Quotient (AQ). The SQ was employed to measure individual differences in trying to understand, analyze, predict, control, and construct rule-based systems. The EQ, which has been proved largely independent of SQ, was employed for measuring individual differences such as specific essential components of social cognition, especially interpersonal reactivity. The AQ was employed for individual differences in autistic traits; however, this score may be predicted from EQ and SQ 21) . The questionnaire consisted of 150 questions, and the response was on a scale of 1 to 4. This component of social ability ─ empathizing ─ is related to cognitive ability in the ToM, which refers to not only understanding the otherʼs state but also predicting or anticipating the otherʼs intention and feelings.
Another component of social ability was memory span as one of the quantified indices of working memory. Working memory required for a wide range of social functioning is supposed to fulfill a dominant role in social functioning. We measured memory span, using the Japanese version of the RST. In the RST, using the computer monitor, each subject read aloud a set of 13-to 16-word sentences, and recalled all underlined words in each sentence at the end of the set. The set size ranged from two to five sentences, and the test consisted of 20 sets. We obtained four parameters using the RST score: the total words, the proportion of words, the correct sets of words, and the truncated span 22) 23) .

fMRI session
Experimental tasks. In order to counterbalance the condition order, we prepared two groups of subjects, one group performing one-person coordination exercises first, and then two-person coordination exercises, and the other group performing the two-person exercises first, then one-person exercises after the fMRI session. In other words, all of the subjects performed either one-person coordination exercises or two-person coordination exercises after the fMRI session. First, the subjects carried out block-designed cognitive tasks containing affective visual stimuli in the MRI system. Then they got out of the MRI system and performed oneperson or two-person coordination exercises for 6 minutes. Furthermore, just after the exercises, they were retested using the same types of the affective stimuli in the MRI system. The six types of oneperson coordination exercises used in this session were: 1. open/close jump, 2. jump with the left leg, then open, and then jump with the right leg, and repeating the same pattern, 3. stretching each hand in different directions, while walking, 4. touching each foot with a different hand in front and at the back, and repeating the same pattern, 5. doing scissors-paper game with legs in the same position, and 6. open/close jump with touching both palms above the head and then touching the thigh twice with the palms. The six types of coordination exercises used in this study were the ones which integrate the five coordination abilities ─ rhythm, balance, control, reaction, and cognitive abilities. The two-person coordination exercises used in these sessions were the same types of exercises, the only difference being that the subjects needed to move in harmony with the rhythm of their partners. Each subject performed 30 seconds of each type of the exercises, then rested for 30 seconds, and then moved to the next type of the exercises; the total duration of the exercises in each session being 6 minutes.
The affective visual stimuli employed here contained pictures of animals, everyday objects (e.g. bicycle, glasses), and facial expressions of human beings. Those pictures of animals and everyday objects were obtained from the Internet or other copyright-free sources. Equal numbers of unpleasant (e.g. insects, snakes, reptiles), pleasant (e.g. dogs, cats, fish), and neutral (everyday objects) stimuli were prepared. The pictures of affective facial expressions were obtained from Pictures of Facial Affect 24) . Equal numbers of pictures of unpleasant (fear, disgust), pleasant (happy), and neutral facial expressions were prepared. The affective components of stimuli were validated by the previous studies 25) 26) . We employed the affective stimuli task to find out how cognitive empathy examined in the social ability session is related to emotion measured in the affective stimuli task.
Each stimulus was presented against a white background that subtended a visual angle of 5.4°× 5.4°. The stimulus duration was 3,000 ms and the onset-to-onset interval was 3,750 ms. The imaging session consisted of 96 stimuli in total (120 TR/ 360 sec). Stimuli of 6 categories including 3 (unpleasant, pleasant, neutral)× 2 (animals/object, faces) categories were presented with 2 cycles, and no stimulus was repeated within a session. Each session included 12 blocks lasting 30 sec, including 8 stimuli of a specific category.
The subjects were asked to pay attention to the pictures, but no overt or covert response was required in reaction to any stimulus.
Image acquisition. The imaging session of each task consisted of 12 blocks with a duration of 30 s (10 TR), each of which consisted of a specific stimulus category presentation, with 4 cycles × 3 categories (120 TR/360 s in total). Images were acquired using a 3.0 Tesla PHILIPS Achieva Quaser Dual ® with a 32-channel coil (SENSE-Head-32P ® ) at Juntendo University Hospital, Tokyo. The subjectʼs head was positioned along the canthomeatal line and immobilized. T1-weighted sagittal scans were used to select 13 contiguous axial slices covering the entire cortex. Functional images were acquired using a gradient-echo echoplanar sequence (TR = 3,000 ms TE = 45 ms, Matrix = 96 × 96, Slice thick-ness = 8 mm, Gap = 1.0 mm, Slice # = 13, FOV = 260 mm, Flip angle = 70°). Prior to each image scan, images equivalent to 2 TR (6 s) were acquired and discarded to allow longitudinal magnetization to reach equilibrium. High-resolution anatomical images for these 13 slices were acquired using a T1weighted sequence (TR = 500 ms, TE = 14 ms, a = 90°, NEX = 2, Slice thickness = 8 mm, In-plane resolution = 0.78125 × 0.78125 mm).
Image processing. Imaging data were preprocessed and voxel-based statistical analysis was preformed using the SPM8 software (Wellcome Department of Imaging Neuroscience) running on MATLAB (version 8.3.0, Math Works Inc., 2014). The first four volumes were discarded, and the remaining 296 volumes were preprocessed. Preprocessing steps before statistical analysis included slice time correction, motion correction, and spatial normalization to a standard template in Montreal Neurological Institute (MNI) space. The slice timing was corrected according to the slice order. The fMRI data were realigned and subsequently normalized to the standard MNI template using the T1 SPM template and resulting in voxels of 2 × 2 × 2 mm. All functional images were spatially smoothed using a Gaussian filter kernel (full width at half maximum [FWHM]= 8 mm). The fMRI data were bandpass filtered (0.008-0.09 Hz). Image artifacts originating from head movement were handled using the ART scrubbing procedure (www.nitrc.org/project s/artifact_detect/). Signal contributions from white brain matter, cerebrospinal fluid, and micro headmovement (six parameters) were discerned from the data. To correct for signal changes caused by head movement, the six realignment parameters were included in the design matrix.
A block design examining responses to a series of stimuli with identical categories and contrasting between stimulus categories was modeled using the standard hemodynamic response function. We reorganized the 6 stimulus categories into 3 (unpleasant, pleasant, neutral) combining animals/ object and faces for the purpose of increasing the S/N contrast and statistical significance. Individual participant images were analyzed at the first level to produce estimates for the contrast of interest (pleasant and/or unpleasant stimuli versus neutral ones) according to the general linear model (GLM), Sudo M, et al: Effects of coordination exercises on social functioning and significant signal changes for the contrast were assessed using F-statistics on a voxel-by-voxel basis. The resulting set of voxel values for the contrast constituted statistical parametric mapping (SPM) of the F-statistic. Contrast images were then analyzed at the second level in a group randomeffects analysis using a one-sample t-test. Furthermore, correlation analysis was also performed between BOLD activities and other factors including results of reading span test (RST) or scores of SQ, EQ, and AQ [threshold significance set at p < 0.05, familywise error (FWE) corrected]. The activated images were superimposed on the standardized T1-weighted images. The MNI (Montreal Neurological Institute) coordinates of the maximum response in the activated regions presented in SPM8 were converted to Talairach coordinates by algorithm 27) . Talairach labels of activated regions were detected and their Brodmann areas (BAs) were determined using Talairach software, client version 2.4.2 (http://www.talairach.org/client. html).

Results
The overall and gender-segregated mean scores of social abilities, SQ, EQ, and AQ were calculated, respectively (Table-2). None of the scores were deviated from the typical scores in the general population 28) 29) . The overall and female correlation analysis revealed that scores of SQ, EQ, and AQ were independent of each other, but there appeared a significant positive correlation between SQ and EQ in the male subjects.
Regarding blood oxygenation level dependent (BOLD) activation evaluated by fMRI, before the two-person coordination exercises, subjects showed significant activations in the right fusiform gyrus (Figure-1A) (Table-3). Similar activations were observed in contrasts of the unpleasant and pleasant stimuli with neutral ones (not shown in a figure) ( Table-3). On the other hand, after the two-person coordination exercises, subjects showed significant activations in the left inferior frontal gyrus during viewing affective stimuli in contrast of the unpleasant stimuli with neutral ones (Figure-1C, Table-3). The BOLD activity during viewing affective stimuli (contrasting unpleasant stimuli versus neutral ones) after the two-person coordination exercises significantly correlated with the RST rate in the right anterior cingulate gyrus (Figure-2, Table-4). We obtained no significant correlation with scores of other items of EQ, AQ or SQ.

Discussion
Among the scores of social abilities, SQ, EQ, and AQ, the results of the data analysis showed that SQ positively correlated with EQ in the male group. This result, which is in accordance with the preceding studies 21) , suggests the necessity of further gender-segregated analysis on the fMRI data related to social functioning.  Before performing the coordination exercises, in the affective-visual-stimuli task we observed the activation in the visual-recognition area, including the lingual gyrus, or face-recognition area, such as fusiform gyrus 30) 31) . These findings simply reflect the visual effects of the pictures we employed as stimuli, which consisted of everyday objects, animals, or faces. After performing the two-person coordination exercises, we observed the activation for affective visual stimuli, particularly for the pleasant stimuli, in the left inferior frontal gyrus. This area connects to frontolimbic regions involved in emotional regulation 32) , and is considered to be one of the loci of language function 33) . This finding claims the hypothesis that coordination exercises activate these social functioning.
Another finding to be noted is that the right anterior cingulate correlated with the RST rate or an index of partial working memory function. The central function of the ToM is located in the frontal Sudo M,    gyrus, such as the anterior cingulate 34)-36) . Therefore, the working memory function and the ToM are closely related. The results of this paper showed that the coordination exercises activate both these functions.
Here we should consider some limitations of the present study. No quantitative control was done on respective loads of social functions over one-and two-person exercises. Present tests on ToM do not include overt cognitive empathy. Due to block design, temporal interplay among the active regions is unclear. The task of evaluating ToM employed in the present study, passive viewing of affective stimuli, might not control the vigilance and concentration of the subjects, nor directly reflect their ToM functions.
This study attempted to find out the specific brain areas underlying social functioning. We were able to provide evidence for the effect of performing coordination exercises on the activation of the left frontal gyrus related to social functioning such as emotion, intention, and motivation. We could also provide support for the hypothesis that two-person coordination exercises activate both the working memory function and the ToM function. The present study suggests that coordination exercises can contribute to interpersonal fields such as coaching for people of all ages through their effects on language abilities, empathy, and working memory in social cognition. Further, this study shows the possibility of the use of gender-specific coordination exercises as movement therapy for enhancing more detailed social functioning. In a future study, we plan to investigate the effect of coordination exercises in preventive medicine in fields such as dementia and depression. The BOLD activity during the viewing of affective stimuli (contrasting unpleasant stimuli versus neutral ones) after the two-person coordination exercises significantly correlated with the RST rate in the right anterior cingulate gyrus.

Region
Talairach coordination (X, Y, Z) of peak location