Neural Mechanism Of Coordination And Enhancement Of Coordinative Ability By Hyper Transcranial Electrical Stimulation

Background The exponential growth of information in the modern military environment has exceeded the cognitive capacity of individuals,necessitating an increasing reliance on collaborative efforts for equipment operation and task execution.As the fundamental driving force for species reproduction and even evolution in nature,there are still many questions regarding the neural mechanism of coordination and its behavioral evolution,which hinders the in-depth understanding and promotion of collaboration among military personnel.Most previous studies have focused on coordinative behavior and observed changes in neural activity,and which makes it difficult to clarify whether the potential neural mechanisms(Inter-brain synchronization(IBS)and activation of Mirror neuron system(MNS))are causal to behavioral performance.Top-down modulation of multi-brain transcranial electrical stimulation or Hyper-transcranial electrical stimulation(Hyper-tES)combined with functional near-infrared spectroscopy(f NIRS)hyperscanning provides the possibility to resolve the causality and promote collaborative performance.From the perspective of network,the coordination between individuals and the core cognitive ability are both important for the interpersonal network.Therefore,it is necessary to explore the individual transfer of effect of coordinative enhancement by hyper-tES.Most of the evaluation of collaborative behavior has low ecological validity.At present,there is a lack of evaluation tools for military collaboration ability in military context.Repetitive multiple brain Transcranial direct current stimulation(t DCS)/Transcranial alternating current stimulation(t ACS)intervention generally induces higher cumulative effects.Exploring the characteristics of short-term and long-term cumulative effects on coordination under the regular intervention has become an effective thrust to shift this research from laboratory mechanism to practical application.Therefore,this study uses hyper-tES combined with f NIRS hyperscanning to reveal and verify the potential brain mechanism of coordination,and explores the transfer effect of stimulation benefits on core cognitive ability at the individual level through monitoring behavior and brain function.Additionally,we aim to construct a high ecological validity task as a training tool for military coordination ability.It is crucial to find regularity and after-effect of 10 repeated hyper-tES intervention on military collaboration,which provides a training basis for sustainedly improving the level of collaboration and ensuring the performance of military personnel on complex tasks.MethodsThis study was divided into three parts and seven studies,all of which used healthy male soldiers as experimental subjects.The details of methods of the three parts were as follows.Part Ⅰ: 124 subjects were randomly divided into hyper-t ACS group,hyper-t DCS group,and sham group.Two active hyper-tES interventions were administered simultaneously to the right Inferior frontal gyrus(IFG)of two individuals in each dyad(hyper-t ACS: 1.5 m A,20 Hz,10 min;hyper-t DCS: 1.5 m A,10 min).Behavioral changes in three stages of stimulation(prestimulation,during stimulation,and poststimulation)were assessed using the joint key-press response task.An experimental cap compatible with f NIRS photoelectrode and tES electrode was developed.The f NIRS was used to continuously monitor the concentration of Oxy-hemoglobin(Hb O)in the task state and rest state of the right IFG and Prefrontal cortex(PFC)around the frontal pole during the stimulation process.A mixed-design ANOVA was performed with IBS and activation degree as indicators.Part Ⅱ: A total of 229 subjects(105 in study III and 124 in study IV)were enrolled and randomly divided into a t ACS group,a t DCS group,and a sham group in each study.(The subjects in this part overlapped with those in Part I and Part III.t ACS/t DCS was used to modulate with the right IFG of the subjects(parameter settings were consistent with the Part I),and the three sub-components of executive functions(working memory,inhibition and cognitive flexibility)were used to quantify behavioral performance before and after stimulation.The accuracy,reaction time,Stroop effect and switching cost were used as indicators for mixed-design ANOVAs.The rest state hemodynamic indexes during tES intervention were simultaneously detected by f NIRS.The Functional connectivity(FC)and activation degree were used as indicators for mixed-design ANOVA or one-way ANOVA.Part Ⅲ: Based on the formation coordinative flight mechanism,the software was designed and made for testing and training of military coordination ability.78 subjects were included to conduct the scale test and completed the operation experience questionnaire survey at least one month before and after the test.A total of 88 subjects were randomly divided into hyper-t ACS group,hyper-t DCS group and sham group.The hyper-tES intervention was repeated 10 times(the other parameters were set the same as Part I),and the changes of the participants at three phases(prestimulation,the first posttest,the second posttest)were monitored by the joint key-press task and the software designed in Part II.The mixed design ANOVA was conducted with the number of coordination wins,reaction time cost,and the highest score or level as indicators.A one-way ANOVA was conducted on the the improvement increment of winning times compared with that in a single hyper-tES intervention.Meanwhile,f NIRS hyperscanning was used to continuously monitor the Hb O concentration of the right IFG and PFC during the whole stimulation process.The IBS,activation degree and FC were used as indicators for mixed-design ANOVAs.ResultsPart Ⅰ: There were no significant differences in the confounding factors that might affect the experimental results among groups,such as basic demographic information,stimulus blinding effect,motivation of participation,tendency of cooperation/competition and interpersonal trust(Ps > 0.05).In the post-stimulation phase,the hyper-t ACS group showed a significant change in the number of wins in block 6(P < 0.001),while the hyper-t DCS group showed no sustained positive change.However,the absolute value of the mean RT difference and the mean RT sum in block 6 of the hyper-t DCS group were significantly higher than those in the sham group(Ps < 0.01).No such significant change in RT was observed in the hyper-t ACS group.This suggests that a single hyper-t ACS intervention improves collaboration better than hyper-t DCS.IBS of task state in the PFC was significantly higher in the hyper-t ACS group than the other two groups in block 5(Ps < 0.05),implying that the increase in IBS continued from block 4 to block 5 in the hyper-t ACS group but not in the hyper-t DCS and sham groups.IBS of rest state in the right IFG was significantly higher in the hyper-t ACS group than that in the hyper-t DCS group(P < 0.05);the above results indicate that the IBS in the PFC of hyper-t ACS is task dependent,but the IBS in the right IFG of hyper-t ACS is task independent.In addition,task-related IBS was only significant in the PFC,and task-related IBS was not significantly changed in the right IFG stimulated by hyper-tES.Pearson correlation analysis showed that IBS in the PFC at block 4 was significantly positively correlated with IBS in the right IFG in the hyper-t ACS group(r = 0.575,P = 0.018),which was not observed in other groups or stages.Thus,the improvement in task-related IBS induced by hyper-t ACS during stimulation may be transferred from the right IFG to the PFC.Pearson correlation analysis showed that IBS in the right IFG or PFC of the real stimulation group was significantly negatively correlated with the absolute value of mean RT difference or mean RT sum(hyper-t ACS group: r =-0.437,P = 0.048;hyper-t DCS group: r =-0.476,P= 0.029),while there was no significant change in the Sham group.IBS was not significantly correlated with the number of wins,and it further indicating the causal relationship between cortex function and coordinative behavior.Part Ⅱ: There were no significant differences in confounding factors such as basic demographic information,blinding effect of stimulation,etc(Ps > 0.05).The Stroop effect(Ps < 0.01)and switching cost(Ps < 0.001)after t ACS/t DCS intervention were significantly lower than those before intervention,and there was no significant change in working memory(accuracy and RT),that is,the behavioral indicators could not distinguish the transfer benefits of the two types of hyper-tES.The significant interaction effect channel pairs of FC were ch 3-ch 10 and ch 7-ch 13.Further analysis showed that the FC of ch 3-ch 10 and ch 7-ch 13 in the t DCS group was significantly lower than that before stimulation(Ps < 0.05),while the other two groups did not show similar changes.In this phase(stimulation),the FC of ch 3-ch 10 and ch 7-ch 13 in the t DCS group was significantly lower than those in the other two groups(Ps < 0.01),which may indicate that the stimulation phase is the critical period(rest state)to distinguish the neural enhancement of the two kinds of tES.Further analysis of activation found that the activation of ch 7 and ch 10 in the t DCS group was significantly lower than those in the sham group during the stimulation phase(Ps < 0.05),and no such significant change was observed in the t ACS group.It indicates the importance of the stimulation phase in distinguishing the transfer effect of hyper-tES.Part Ⅲ: The software for assessing military coordination ability showed satisfactory in terms of fun,understanding difficulty of operation rules,and the demand for players’ coordination ability.Pearson correlation analysis showed that the post-test scores were significantly positively correlated with the pre-test scores(r = 0.655,P < 0.001;r =0.725,P < 0.001),which meant good test-retest reliability.In the study of repeated hyper-tES intervention,there were no significant differences in the confounding factors that might affect the experimental results,such as basic demographic information,stimulus blinding effect,motivation of participation,tendency of cooperation/competition,interpersonal trust and so on(Ps > 0.05).The scores of the software in active hyper-tES group were significantly higher than those in sham group(P < 0.001).The number of wins in blocks 5-6 was significantly higher than baseline(block 1)in the hyper-t ACS and hyper-t DCS groups,but not in the sham group.In block 5 and block 6(the second posttest),the hyper-t ACS/t DCS group had a significant difference in the number of wins compared with the sham group(Ps < 0.05).However,the absolute value of the mean RT difference between the hyper-t ACS/TDCS group at the first posttest was significantly higher than that at prestimulation and the second posttest(Ps < 0.05),while no similar significant changes were observed in the other two groups.This indicates that the hyper-t ACS group may need more time cost in the promotion.Compared with single stimulation session,the increase in the number of wins of multiple active hyper-tES was significantly higher than that of single session(P < 0.05).The increase in the number of wins in the multiple hyper-t DCS group was significantly higher than that in the single hyper-t DCS group(Ps < 0.05),while there was no such change in the hyper-t ACS group,which may be related to the strong task dependence of t ACS.There was no significant interaction effect of IBS among the three groups(Ps > 0.05).In the hyper-t DCS group,the Hb O concentration in the PFC was significantly lower than the other two groups at the second posttest phase.Further Pearson correlation analysis showed that in the hyper-t DCS group,the Hb O concentration in the PFC at the first posttest phase was significantly positively correlated with the Hb O concentration in the right IFG(r =0.555,P = 0.002),which was not observed in the other groups or stages.Therefore,the improvement of task-related activation induced by hyper-t DCS may be transferred from the right IFG to the PFC during stimulation.In the hyper-t DCS group,the channel FC in the PFC at the first/second posttest phase was significantly lower than that in other groups(Ps < 0.05).In the hyper-t ACS group,the channel FC between the right IFG-PFC at the first posttest phase was significantly lower than that at prestimulation or other groups(Ps< 0.05).FC of ch 2-ch 5 at the second posttest phase was significantly decreased compared with that at prestimulation(P < 0.05).Conclusion(1)The enhancement of IBS in the PFC and the increase of neural efficiency in the right IFG are important brain mechanisms for a single session of hyper-tES to promote coordination,and online hyper-t ACS can induce better coordinative improvement than hyper-t DCS.(2)The benefits of hyper-tES stimulation are transferred to the core sub-components of executive functions such as inhibition and cognitive flexibility.The stimulation phase is the key period to differentiate the cognitive transfer effects of hyper-t ACS and hyper-t DCS,and t DCS has a more positive effect on brain function such as activation and functional connectivity.(3)The two repeated hyper-tES interventions can effectively improve the performance of the military personnel.The improvement increment of multiple hyper-t DCS on coordination performance is much higher than that of single session.Hyper-t ACS did not show obvious advantages of repeated intervention.Therefore,hyper-t DCS is the first choice for repeated intervention in offline mode.(4)The enhancement of PFC neural efficiency is the neural mechanism of repeated hyper-t DCS improving collaboration,while repeated hyper-t ACS improves collaboration by affecting FC between brain regions,which is different from the enhancement of IBS induced by single online mode.