Methods for Tracking Dynamically Coupled Brain-Body ...data types and visualization tools, to...

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Methods for Tracking Dynamically Coupled Brain-Body Activities during Natural Movement Jihye Ryu Psychology Dept Rutgers University New Brunswick, New Jersey [email protected] Joseph Vero Biomedical Engineering Dept Rutgers University New Brunswick, New Jersey [email protected] Elizabeth B. Torres Psychology Dept Rutgers University New Brunswick, New Jersey [email protected] ABSTRACT A fundamental property of movement is its dynamically changing variability and its adaptive nature. These features seem to be con- nected to the cognitive control of our actions by the brain. However, it has been a challenge to connect cognitive neuroscience and move- ment science in developing a framework amenable to study the coupled dynamics of the brain and body during natural movements. Part of the problem has been the lack of proper sensors to probe both activities in tandem. Fortunately, contemporary advances in wireless technology with high sampling resolution have paved the way to address this challenge. In this paper, we make use of wire- less wearable sensors and a new statistical platform to study the dynamic interactions of the brain, body and heart during natural walking. To examine the influence of cognitive tasks on deliberate (self-emergent), spontaneous, or inevitable (autonomic) processes, we combine the use of a metronome and specific instructions on paced breathing, while harnessing the heart signal underlying the evoked behaviors. This paper presents a new platform for the in- dividualized behavioral analyses, which incorporates a new set of data types and visualization tools, to quantify the outcome of such experimental paradigm. We discuss our results and suggest that these new methods and paradigm may serve to unify and advance the fields of cognitive neuroscience and neuro-motor control. CCS CONCEPTS Mathematics of computing Distribution functions; Ap- plied computing Systems biology; KEYWORDS graphical network analysis, weighted directed graph, network con- nectivity, stochastic analysis, brain-body interface, gait ACM Reference format: Jihye Ryu, Joseph Vero, and Elizabeth B. Torres. 2017. Methods for Tracking Dynamically Coupled Brain-Body Activities during Natural Movement. In Proceedings of MOCO ’17, London, United Kingdom, 28-30 June, 2017, 8 pages. https://doi.org/http://dx.doi.org/10.1145/3077981.3078054 Permission to make digital or hard copies of all or part of this work for personal or classroom use is granted without fee provided that copies are not made or distributed for profit or commercial advantage and that copies bear this notice and the full citation on the first page. Copyrights for components of this work owned by others than ACM must be honored. Abstracting with credit is permitted. To copy otherwise, or republish, to post on servers or to redistribute to lists, requires prior specific permission and/or a fee. Request permissions from [email protected]. MOCO ’17, 28-30 June, 2017, London, United Kingdom © 2017 Association for Computing Machinery. ACM ISBN 978-1-4503-5209-3/17/06. . . $15.00 https://doi.org/http://dx.doi.org/10.1145/3077981.3078054 1 INTRODUCTION Recent advances in wireless technology have opened new avenues to translate basic research into applications to performing arts, sports, and clinical fields among others. Amidst this transformative era, we have introduced a new statistical platform for the individu- alized behavioral analyses (SPIBA) [11] and derived new data types amenable to study the dynamically coupled brain-body activities during performance of natural movements [13]. Using this platform, we are able to examine the fluctuations in amplitude and timing of biophysical rhythms that are continuously output by the nervous systems during natural activities. These rhythms may come from disparate layers of the peripheral and central nervous systems (PNS and CNS) ranging from autonomic to spontaneous to voluntary levels [4]. Owing to their complexity, such as the different frequency ranges and spatio-temporal scales, multiple biophysical signals have been difficult to study in tandem so as to pose new questions on the brain-body closed-loop performance. Indeed, there is a paucity of work that examines the dynamically coupled brain-body activity. Moreover, the extant literature on this topic smooths out the wave- forms of interest through averaging under Gaussian, linearity and static (stationary) assumptions. As such, there is gross data loss that prevents us from better understanding the PNS-CNS interactions. In this sense, it may be argued that most science is either about a “disembodied brain” or a “brainless body”, which is often studied by observation using descriptions of unambiguous, overt bodily motions. Such an approach tends to constrain the focus on aspects of goal-directed behavior and leave out the spontaneous/inevitable aspects of the performance, which often occurs largely beneath our conscious awareness [6]. We simply do not know how such spontaneous activity (that we smooth out as “noise” or nuisance) emerges and contributes to the autonomy of our brain exerting over the body in motion. Other challenges we face when recording brain-body activity may include misalignment of temporal landmarks from different ac- quisition systems and motor artifacts corrupting cortically-related signals. New wireless technology and collaborative work among scientists and industry have created and maintained an open access platform (e.g., lab streaming layer, LSL) that enables integration of signals from different instruments, while motion-artifact removal from cortical signals are also gaining traction [2]. The present work combines new advances in data acquisition, multilayered data pro- cessing, statistical analyses and cognitive neuroscience to introduce a new platform for the personalized study of dynamically coupled brain-body activities during natural movements.

Transcript of Methods for Tracking Dynamically Coupled Brain-Body ...data types and visualization tools, to...

Page 1: Methods for Tracking Dynamically Coupled Brain-Body ...data types and visualization tools, to quantify the outcome of such ... Participants were instructed to walk at their own comfortable

Methods for Tracking Dynamically Coupled Brain-BodyActivities during Natural Movement

Jihye RyuPsychology DeptRutgers University

New Brunswick, New [email protected]

Joseph VeroBiomedical Engineering Dept

Rutgers UniversityNew Brunswick, New Jersey

[email protected]

Elizabeth B. TorresPsychology DeptRutgers University

New Brunswick, New [email protected]

ABSTRACTA fundamental property of movement is its dynamically changingvariability and its adaptive nature. These features seem to be con-nected to the cognitive control of our actions by the brain. However,it has been a challenge to connect cognitive neuroscience and move-ment science in developing a framework amenable to study thecoupled dynamics of the brain and body during natural movements.Part of the problem has been the lack of proper sensors to probeboth activities in tandem. Fortunately, contemporary advances inwireless technology with high sampling resolution have paved theway to address this challenge. In this paper, we make use of wire-less wearable sensors and a new statistical platform to study thedynamic interactions of the brain, body and heart during naturalwalking. To examine the influence of cognitive tasks on deliberate(self-emergent), spontaneous, or inevitable (autonomic) processes,we combine the use of a metronome and specific instructions onpaced breathing, while harnessing the heart signal underlying theevoked behaviors. This paper presents a new platform for the in-dividualized behavioral analyses, which incorporates a new set ofdata types and visualization tools, to quantify the outcome of suchexperimental paradigm. We discuss our results and suggest thatthese new methods and paradigm may serve to unify and advancethe fields of cognitive neuroscience and neuro-motor control.

CCS CONCEPTS•Mathematics of computing→Distribution functions; •Ap-plied computing→ Systems biology;

KEYWORDSgraphical network analysis, weighted directed graph, network con-nectivity, stochastic analysis, brain-body interface, gait

ACM Reference format:Jihye Ryu, Joseph Vero, and Elizabeth B. Torres. 2017. Methods for TrackingDynamically Coupled Brain-Body Activities during Natural Movement. InProceedings of MOCO ’17, London, United Kingdom, 28-30 June, 2017, 8 pages.https://doi.org/http://dx.doi.org/10.1145/3077981.3078054

Permission to make digital or hard copies of all or part of this work for personal orclassroom use is granted without fee provided that copies are not made or distributedfor profit or commercial advantage and that copies bear this notice and the full citationon the first page. Copyrights for components of this work owned by others than ACMmust be honored. Abstracting with credit is permitted. To copy otherwise, or republish,to post on servers or to redistribute to lists, requires prior specific permission and/or afee. Request permissions from [email protected] ’17, 28-30 June, 2017, London, United Kingdom© 2017 Association for Computing Machinery.ACM ISBN 978-1-4503-5209-3/17/06. . . $15.00https://doi.org/http://dx.doi.org/10.1145/3077981.3078054

1 INTRODUCTIONRecent advances in wireless technology have opened new avenuesto translate basic research into applications to performing arts,sports, and clinical fields among others. Amidst this transformativeera, we have introduced a new statistical platform for the individu-alized behavioral analyses (SPIBA) [11] and derived new data typesamenable to study the dynamically coupled brain-body activitiesduring performance of natural movements [13].

Using this platform, we are able to examine the fluctuations inamplitude and timing of biophysical rhythms that are continuouslyoutput by the nervous systems during natural activities. Theserhythms may come from disparate layers of the peripheral andcentral nervous systems (PNS and CNS) ranging from autonomicto spontaneous to voluntary levels [4].

Owing to their complexity, such as the different frequency rangesand spatio-temporal scales, multiple biophysical signals have beendifficult to study in tandem so as to pose new questions on thebrain-body closed-loop performance. Indeed, there is a paucity ofwork that examines the dynamically coupled brain-body activity.Moreover, the extant literature on this topic smooths out the wave-forms of interest through averaging under Gaussian, linearity andstatic (stationary) assumptions. As such, there is gross data loss thatprevents us from better understanding the PNS-CNS interactions.In this sense, it may be argued that most science is either about a“disembodied brain” or a “brainless body”, which is often studiedby observation using descriptions of unambiguous, overt bodilymotions. Such an approach tends to constrain the focus on aspectsof goal-directed behavior and leave out the spontaneous/inevitableaspects of the performance, which often occurs largely beneathour conscious awareness [6]. We simply do not know how suchspontaneous activity (that we smooth out as “noise” or nuisance)emerges and contributes to the autonomy of our brain exertingover the body in motion.

Other challenges we face when recording brain-body activitymay include misalignment of temporal landmarks from different ac-quisition systems and motor artifacts corrupting cortically-relatedsignals. New wireless technology and collaborative work amongscientists and industry have created and maintained an open accessplatform (e.g., lab streaming layer, LSL) that enables integration ofsignals from different instruments, while motion-artifact removalfrom cortical signals are also gaining traction [2]. The present workcombines new advances in data acquisition, multilayered data pro-cessing, statistical analyses and cognitive neuroscience to introducea new platform for the personalized study of dynamically coupledbrain-body activities during natural movements.

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Figure 1: New coupled brain-body paradigm to assess thePNS-CNS closed loops interactions. ©E.B.Torres

2 EXPERIMENTAL AND COMPUTATIONALDETAILS

2.1 A Natural Task: Spontaneous/Inevitable vs.Deliberate behavior

Participants were instructed to walk at their own comfortable pacefor 12-15 minutes under three different conditions: (1) Under thecontrol condition, participants simply walked around the roomas they naturally do; (2) Under the metronome condition, theywalked while listening to a metronome beat at 12 times per minute.They were not instructed to do anything about it (hypothesizingspontaneous emergence of responses linked to the metronome); (3)Under the paced breathing condition, the participant was instructedto walk while listening to the metronome beat at the same speed,and to deliberately control their breathing pace. Specifically, eachparticipant was instructed to inhale at the first beat and exhaleat the second beat, thus completing six cycles of breath at eachminute (Fig.2A). This condition was hypothesized to change thepatterns of brain-body coupling and shift heart rhythms in relationto conditions (1) and (2).

2.2 Data Acquisition and Signal Processing2.2.1 Instrumentation Specs. The participant wore three differ-

ent types of wireless sensors to harness biorhythms from the CNSand PNS. For the CNS we used electroencephalography (EEG) sen-sors. For the PNS we used electro cardiogram (ECG) and motionsensors.

The cortical potentials were captured using the Enobio wirelessEEG device (Barcelona, Spain) at 500Hz sampling rate with 32 sen-sors positioned across the scalp. The EEG recording device waspositioned on the back of the participant’s head (yellow device InFig.2B center), which contains an inertial measurement units (IMU)that records head acceleration at 500Hz. Data from this device wererecorded by NIC Neuroelectrics (Barcelona, Spain). The accelera-tion of the participant’s bodily motion was captured using OpalIMUs (APDM Inc., Portland, OR) at 128Hz sampling rate, and wereacquired with Motion Studio (APDM Inc., Portland, OR). Partici-pants wore ten opal IMUs with Velcro belts on the wrists, ankles,

Figure 2: Experimental paradigm and sensors. (A) Three con-ditions: natural walk (control), metronome (spontaneousload) and instructed paced breathing (deliberate load). (B)Sensors: IMUs and their locations showing the nodes of thePNS network; EEG and the locations showing the nodes ofthe CNS network; ECG and the sensor’s locations. ©J.Ryu

foot, upper arm on both right and left sides, and on the posteriortrunk and anterior chest (Fig.2B). The heart signals were obtainedfrom a wireless Nexus-10 device (Mind Media BV, The Netherlands)and Nexus 10 software Biotrace (Version 2015B) at a sampling rateof 256Hz. Three electrodes were placed on the chest according tothe standardized lead II method, and were attached with adhesivetape (Fig.2B).

2.2.2 Lab Stream Layer (LSL) Use. In order to temporally syn-chronize the signals obtained from the three devices–EEG, ECGsensors, and Opal IMUs, an open source package LSL was used.Among the applications contained in LSL, LabRecorder and Mousewas used so that the EEG data streams would be event-marked bymouse clicks made on the display screen of the computer, fromwhere the softwares interfacing the sensor devices (e.g., MotionStudio, NIC, and Biotrace) were running.

2.2.3 Pre-processing. Acceleration data obtained from the OpalIMUs and ECG heart data were up-sampled to 500Hz using cubicspline interpolation, so that they would later be analyzed at thesame sampling rate as the EEG brain potential data.

EEG data was properly band passed to remove 60Hz AC current.Traditional ICA-based methods are used to detect periodic eye-motions (e.g. blinks) and facial (e.g. jaw-related motion) patterns inthe waveforms [1]. Here, we incorporated new analyses specificallyinvolving head motions, where the output from an IMU embeddedin the head cap was used to detect head jerks (rate of change of ac-celeration) and their coherence patterns with the rates of change ofthe EEG-signal were tracked. Specifically, the EEG data were bandpassed at 16-31Hz (i.e., beta frequency band) and coherence analy-ses of the two data’s rate of change were examined. Accelerationpeaks of head jerks were followed by peaks of change in corticalsignals at the beta band frequency after approximately 40ms, im-plying that these cortical signals reflected head motion artifacts.Hence, when 0.1% highest peaks of head acceleration (i.e., headjerks) occurred, the acceleration signals were compared against thebeta band cortical signals via cross correlation, and if the corticalsignals lagged the head acceleration peaks, these instances were

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excluded. Overall, this resulted in eliminating approximately 0.001%of the entire data.

Subsequently, the cortical data from each channel were refer-enced by the channel that had the least noise. Specifically, for eachchannel, the peaks extracted from the fluctuations in the amplitudeof the cortical waveform were studied as a Gamma process (seesection 2.3.2) and the channel with the lowest scale value (i.e. lowestnoise to signal ratio, NSR) was chosen to have the lowest noise andwas set as the reference. Indeed, there are many artifacts in thecortical signals that are traditionally removed by hand and visualinspection, and generally cannot be fully eliminated. Given the mas-sive amount of data we continuously track here, hand-visualizationanalyses were not feasible. In that sense, our introduction of au-tomatic assessment of noise and re-referencing to a channel withthe least NSR are our best bet to reduce the impact of such arti-facts while implementing it in an automated way. The rationalebehind this approach is further explained in the following sections2.3.1-2.3.3.

2.3 Statistical Platform for IndividualizedBehavioral Analysis

2.3.1 Waveforms. Raw biophysical data that are continuouslyregistered from physiological sensors (i.e. data derived from physio-logical rhythms) such as bodily kinematics, electroencephalography(EEG), electrocardiogram (ECG), electromyography (EMG), respi-ration patterns, etc., give rise to a time series of peaks and valleys.Their fluctuations properly normalized as in (equation 1) producespike trains (coined “the micro-movements” [8, 10]) that we treatas a random point process (Fig. 3A-B):

NormPeak =Peak

Peak +Avrдmintomin(1)

In a series of micro-movements, the order of the original signal’samplitude peak values is preserved, but the frame/time values arelost. To recover all the frame values and preserve the samplingresolution of the original signal, we set the non-peak values to0 and superimpose the micro-movements (i.e., normalized peakamplitude) on the original frames. An example of a spike train inthe original frame order is shown in Fig.3C, which is based on themicro-movements signal (Fig.3B) extracted from the raw data signal(Fig.3A). Note, this is done for all sensors’ signals, thus allowing usto integrate them from different levels of the nervous systems, e.g.the CNS (EEG-spikes) and the PNS (motion-spikes).

2.3.2 SPIBA: using aGamma Process. The spike trains are treatedunder the assumption of independently identically distributed (I.I.D.)events, representing a continuous random process under the gen-eral rubric of a Poisson Random Process, where events in the pastmay (or may not) accumulate evidence towards prediction of futureevents (see also [6–11] for various examples to different nervoussystem’ biorhythms). These spike trains are used as input to aGamma process to empirically estimate the Gamma parameters (e.g.using maximum likelihood estimation with 95% confidence inter-vals) [10, 11]. The estimated shape and scale parameters are trackedon the Gamma parameter plane (where the vertical axis representsdistribution’s dispersion/scale parameter, and the horizontal axis

Figure 3: SPIBA andWeighted Directed Graphs. (A) Raw bio-physical signal (e.g. IMU’s acceleration, EEG or IBI-time se-ries) are resampled at equal rates. (B) Micro-movements (i.e.,moment to moment fluctuations in signal amplitude nor-malized between 0 and 1; see text) in the peak order. (C)Spike-trains from micro-movements in the original frameorder. (D) Two signals normalized as in (B-C steps) from dif-ferent sensors (left parietal node on top, and rightwrist nodeon the bottom) are subject to power spectral analyses. (E)Cross-coherence analyses produce pairwise coherence pro-files and lead-lag information across frequencies. (F) Coher-ence, phase and frequency matrices. (G) Coherence, phaseand frequencymatrices where the node from row i leads thenode from column j. This is later used to build weighted di-rected graphs and perform network connectivity analyses.(H) Brain, body and brain-body coupled networks represent-ing the networks’ state for a single minute. This can be dy-namically tracked over the 12-15minute sessions.

represents the distribution’s skewness/shape parameter). Theseestimated parameters are further used to estimate the spike train’sGamma probability distribution functions (PDF) and its moments,to profile noise-to-signal transitions inherent in the multilayered,dynamically evolving biophysical data.

2.3.3 Statistical Inference. The above-mentioned Gamma pa-rameter plane provides information on the noise to signal ratio(NSR), which is equivalent to the scale parameter value of the es-timated Gamma PDF [3]. Thus, higher noise will correspond toa higher value along the vertical axis on the Gamma plane (i.e.,scale axis). It is also important to emphasize that when the esti-mated shape parameter a of the PDF equals a=1, the data follows amemoryless Exponential PDF. This is the most random distributionwhereby events in the past do not accumulate information predic-tive of future events [3]. Larger values across the horizontal axisof the Gamma plane (i.e., shape axis) represents PDFs with moresymmetry, with a variety of skewed distributions between the twoextremes. These statistical features enable direct inference fromthe moment by moment fluctuations in the biophysical signals thatare continuously output by the nervous systems. As such, they al-low interpretations of natural behaviors under different conditions

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(such as natural gait studied here under spontaneous and deliberateconditions described in section 2.1)

2.3.4 Central and Peripheral Networks. In order to analyze theinteractions that occur across the brain and body, spike trains ofeach sensor data (which we will refer to as ‘nodes’ from hereon)were examined in terms of nodes that comprise a large network,made up of brain-related and the body-related sub-networks. Theidea introduced here is to use network connectivity analyses com-monly used in brain science [5] and extend it to the study of periph-eral networks introduced by our group to study natural movementssuch as gait and reach [12]. To that end, we will present severalexamples of the use of this framework to dynamically track thebrain-body coupled network. (Note that we can track the individualsubnetworks of the brain and the body as well, but due to spaceconstraints, we will focus on the brain-body coupled network inthis paper.)

First, all spike train data were separated by 1 minute worth oftime series at 500Hz to provide a minute-by-minute profiling of thebehavior. Then, for each pair of nodes across the brain and bodyduring each minute, cross coherence was computed yielding thecoherence and lead-lag phase values at varying frequencies (Fig.3E).

For each minute, the maximum coherence value was extractedfor each pair of nodes, along with the corresponding phase (viacross spectral power density) and frequency values. These can bevisually represented in the form of matrices as shown in Fig.3F. InFig.3F (left), each entry of the coherence matrix contains the maxcoherence value during a minute time-frame for each pair of nodesrepresented in the rows and columns. Here, the first 31 items of rowsand columns belong to nodes within the brain network, and thenext 11 items belong to nodes within the body network. The phaselead-lag matrix in Fig.3F (middle), contains the phase (degrees)value when the maximum coherence value occurs between thecorresponding pair of nodes. The frequency matrix in Fig.3F (right)contains the frequency value when the maximum coherence valueoccurs between the corresponding pair of nodes. In Fig.3G, thethree matrices are those corresponding to the positive (lead) valuesof the phase lead-lag matrix, where the node from row i leads thenode from column j. The matrices thus obtained are the adjacencymatrices used to build a weighted directed graph representing thefull brain-body network, as shown in Fig 3H. Note, we can furtherdecompose the signal into different frequency bands and providethe analyses described below for each frequency band (e.g. thetraditionally studied alpha, beta, gamma, theta, mu, gamma bands).However, due to space constraints, this paper will use the fullfrequency spectrum to illustrate the methods.

One novel element in our approach (besides extending brain con-nectivity analyses to connectivity analyses of brain-body couplednetworks) is the combination of the micro-movements underlyingthe activity of the node and the SPIBA framework to examine thedynamic evolutions in the node’s stochastic signatures.

2.4 Visualization Tools2.4.1 PNS-CNS Networks. Cross coherence analyses on paired

nodes yielded an adjacency matrix to represent a weighted-directedgraph, which visualizes the network of nodes and their links. InFig.3H, the ‘PNS Network’ graph shows the 11 nodes from the

body and the ‘CNS Network’ graph shows the 31 nodes from thebrain, during a single minute. The arrows show the directionalityof the paired nodes, and the arrow weights represent the phaselevel, where thicker arrows would imply longer lead-lag relation-ship between the two nodes. The edge colors of the node representthe coherence strength specified in the color bar. Based on thecoherence strength and connectivity weights, nodes can be sponta-neously separated into modules (sub-network). To detect them, weuse the modularity metric [5]. Each module maximizes the numberof within-group edges and minimizes between-group edges. Gen-erally, there were 2-3 modules within each minute, and the colorof each node represents the module in which the node is included.See also Fig.4A.

The ‘Coupled Network’ graph in Fig.3H shows all 42 nodesfrom the brain and body, with the same specification rules as the‘PNS Network’ and the ‘CNS Network’ graph. Here, the ‘CoupledNetwork’ graph shows the interaction mainly between the nodesfrom the body and nodes from the brain, where the upper leftportion of the nodes in a circular shape correspond to those in thebrain, and the lower right portion of the nodes in a stick-figureshape correspond to those in the body.

These networks allow us to visualize the dynamic minute-by-minute interactions between each pair of nodes, within the brain,within the body, and between the brain and body. In order to vi-sualize the progression of network connections throughout therecording duration, rather than from a single static minute, minute-by-minute profile of these networks can be exhibited in videos foreach CNS (see video here), PNS (see video here), and and Couplednetworks (see video here).

2.4.2 Reciprocally Connected Network. The network of coher-ence among paired nodes can also be visualized by looking for self-emerging patterns from sub-network (module) synergies within thecoupled network (Fig.4A). During each session of recordings, foreach node, we counted how many minutes that node participatedin a particular module (Fig.4B-top) and computed the proportion oftimes across a condition that a given node stayed in each module(Fig.4B-bottom). If a pair of nodes had the same proportion of timestaying in each module during the entire session (i.e. node i lednode j and node j led node i equal number of times within the mod-ule), then the two nodes were considered reciprocally connected.Thus the network graph can be represented with double arrowspointing in both directions for those reciprocally connected nodes(Fig.4C). Essentially, reciprocally connected pairs of nodes exhib-ited the same pattern of modularity during the recording session,implying synergies between these pairs of nodes.

This visualization allows us to understand the connectivity inregards to self-emerging patterns of coupled brain-body activitydynamically unfolding and changing from session to session.

2.4.3 Additional tools to summarize coupled PNS-CNS modulesas a measure of sub-networks’ togetherness. The modularity metricwas further used to visualize the patterns of brain-body together-ness for each self-emerging module (Fig.5A). Here, we count thenumber of times the node participated in the same module (Fig.5B).Then, we categorize these nodes by regions (e.g. Parietal regionis comprised of nodes in the right/left parietal lobes; Arms region

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Figure 4: Connectivity-Modularity Analyses. (A) Weighteddirected graph for the body-brain coupled network, wherethe pairwise node coherence level is shown in the colorsof the marker edge (see color bar). Based on the coherencelevel, three modules (sub-networks) emerge at minute 15(shown in the colors of marker-face: yellow, cyan and ma-genta) across the brain and body. Directed arrows informthe leading node in each pair. (B) Number of minutes (seecolor bar) each node (x-axis) participated in one of threemodules (y-axis) across a 15min session (top), and the pro-portion of time spent in each module (x-axis) for a singlenode shown in bar-plot (bottom). (C) Reciprocal connectionsbetween brain and body nodes (double arrows). Node colorsignifies the strength of reciprocal connections (i.e., numberof links coming in and out of the node across the session;see color bar). Node size reflects the number of reciprocalconnections the node is involved in (larger nodes indicatehigher occurrence of reciprocity).

contains the right/left upper-arms and wrists). This regional sub-division is arbitrary (i.e., it can be sub-divided in other ways) andallows us to ask how two known regions relate to each other. Foreach region, we examine whether those regional nodes participatedin a certain module for more than half of the maximum time counts(stars are marked on the peaks if they exceed the 1/2 threshold inFig 6A). Then we examine one region from the body and anotherregion from the brain in pairs, to see if the two regions exceededthe ½ threshold (i.e., participated together). If both regions do notexceed the threshold, they would be considered ‘disjointed’. Thiscan be represented in a binary matrix shown in Fig 6B for all threemodules, where yellow indicates the brain-body region together-ness (1) and blue indicates disjoint-ness (0). Fig 7B is a graphicalnetwork representation of Module 1, where the double sided arrowindicates the togetherness between the two regions from the brainand the body.

2.4.4 Summary Statistics Profile. Underlying each node is a sto-chastic signature of spike trains that was mentioned in sections2.3.1-2.3.3. Here, we define the spike train of each node and usethem as input to a Gamma process, where the Gamma parametersare empirically estimated. One way to visualize the statistics ofeach node’s spike trains is a four-dimensional graph, as is shown inFig.10 with the estimated Gamma PDF in the top insets of Fig 10A,10B and the corresponding estimated Gamma parameters plottedon the Gamma parameter plane in the bottom insets of Fig 10A,10B. In the 4D graphs, the empirically estimated mean, variance,and skewness of the fitted Gamma PDFs for each node during eachcondition are plotted on the x, y, and z axes respectively. The size ofthe marker reflects the level of kurtosis, where larger size indicates

Figure 5: (A) Modularity matrices for brain (left), body (mid-dle), and coupled brain-body (right). (B) Number of times (y-axis) each node participated in one of three module (x-axis).

Figure 6: (A) Each node within the brain (left) and body(right) is categorized into regions and relabeled along thex-axis with the initials of the region. The brain nodes arecategorized into 6 brain regions (P: parietal, C: central, T:temporal, F: frontal, PF: pre-frontal, O: occipital) and thebody nodes are categorized into 6 body regions (H: head,W: right/left wrist, T: trunk, L: lumbar, U: right/left upper-Arms, A: right/left ankles, F: right/left feet). The y-axisshows the number of times each node participated in a cer-tain module. If it participated in the same module for morethan ½ of the maximum time count, it is marked with astar. (B) Participation binary matrix, where the rows andcolumns represent regions from the brain and body, andentries are in yellow (1) if the two regions participated to-gether in the samemodule. Otherwise, the entries are in blue(0). The leftmost participation matrix (Module1) representsthose shown in Fig. 6A.

high kurtosis level of the fitted PDF. The colour of the marker is dif-ferentiated across conditions. This graph allows us to visualize thestatistical features of each node and understand how the stochas-ticity changes across different conditions for the brain nodes andfor the body nodes.

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Figure 7: (A) Participation matrix for Module1. (B) Couplednetwork graph of the brain-body togetherness across re-gions, where the double sided arrows represent together-ness.

Figure 8: Weighted directed graph for the brain-body cou-pled network under the control condition (left), metronomecondition (middle) and deliberate paced breathing condition(right) atminute 5. Based on the coherence strength betweenpairs of nodes (shown in the marker edge colors and colorbar), two modules (sub-networks) emerge at minute 5 (dif-ferentiated bymarker-face colors: cyan andmagenta) acrossthe brain and body for all conditions.

3 RESULTS AND DISCUSSION3.1 Spontaneously Emerging Modules in the

Brain-, the Body- and theCoupled-Networks Differentiate CNS-PNSStates

3.1.1 PNS-CNS Networks. For each minute and for each condi-tion, the brain-body coupled network was visualized, and exhibiteddynamic interactions between the brain and body throughout theexperiment. Generally, the nodes self-grouped into 2-3 modules,and the presence of these modules changed throughout the 12-15minutes of recording for all conditions. Fig. 8 shows an exampleof the coupled network at minute 5 for each condition. The pro-gression of the network connections during the entire recordingfor each condition for a representative participant can be viewed inthese videos: control, metronome, and paced breathing conditions.

3.1.2 Reciprocally Connected Network. For each condition, thereciprocal connections of the coupled network were visualized asshown in Fig. 9. For this participant, self-emerging reciprocal con-nections were fairly sparse when the participant was naturallywalking. However as there were additional task loads imposed on

Figure 9: Representative profile of the Reciprocally Con-nected Coupled Network dynamically changing across con-ditions. The density of reciprocal connections increase asthe participant is imposed with additional task - one thatis spontaneous (i.e., metronome condition) and one that isdeliberate (i.e., paced breathing condition).

Figure 10: The 4D statistical summary profile of the brainand body nodes across conditions. (A) Brain nodes. (B) Bodynodes. Insets are the PDF (top) and estimatedGammaparam-eters (bottom) of a representative node at each minute.

walking, from a passive/spontaneous task (i.e., metronome con-dition) to a deliberate task (i.e., paced breathing condition), self-emerging reciprocal connections became denser. It can be construedthat for this participant, as the additional task load increased, theinteractions between the brain and body became more active. Thiswas a pattern generally found across other participants, wherebydifferences in reciprocal connections were found from one condi-tion to the next. The extent and strength of such interactions variedacross individuals.

3.2 Different Noise-to-Signal ProfilesCharacterize Gait under Different Mentaland Autonomic Demands

The stochastic signatures of each node within the entire networkwere examined across all conditions. Fig. 10A shows the estimatedGamma moments for each brain node based on its empiricallyestimated PDF for each condition, which is differentiated by thecolor of themarkers. Fig. 10B shows the estimated Gammamomentsof the nodes belonging to the body. The top insets of Fig. 10A,10B shows the estimated Gamma PDF for each minute for a singlerepresentative node from the brain (Pz node for control condition, F4node for the metronome condition P7 node for the paced breathingcondition) and body (lumbar node for control condition, and rightfoot node for the metronome and paced breathing condition). Thebottom insets of Fig. 10A, 10B shows the estimated scale and shapeparameters in log values plotted on a Gamma parameter plane forthe corresponding node shown in the insets positioned above.

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Tracking Dynamically Coupled Brain-Body Activities MOCO ’17, 28-30 June, 2017, London, United Kingdom

Table 1: Pairwise Kruskal-Wallis Non-parametric Test ofEmpirically Estimated Gamma Parameters between Condi-tions

Parameter Pair χ2 df p-value

Shape Control vs. Metronome 6.28 (1,278) 0.01*Metronome vs. Breathing 0.67 (1,656) 0.41Control vs. Breathing 7.41 (1,544) 0.01*

Scale Control vs. Metronome 5.61 (1,278) 0.02*Metronome vs. Breathing 1.53 (1,656) 0.22Control vs. Breathing 3.92 (1,544) 0.05*

For nodes from both brain and body, the statistics under thenaturally walking condition (control) exhibited systematically in-creasing levels of skewness and kurtosis compared to conditions ofspontaneous metronome and deliberate paced breathing. As such,differences in the estimated Gamma parameters from the naturallywalking condition against the other two conditions were foundto be statistically significant (Table 1) using the pairwise Kruskal-Wallis test. Note, this test was used solely as a comparison of meanranks across conditions so as to gain insights on the range of thefamily of PDFs that the tasks evoked.

3.3 Different ‘togetherness’ patterns acrossbrain and body regions were detectedacross conditions

The examination of togetherness in brain-body regions produceddifferent patterns for each self-emerging module in the networkand for each condition. These can be seen in the patterns of Fig.11,implying change in interactions across different sub-regions of thebrain and body and across different conditions. In Fig.12, these pat-ternswere summarized by bar-plots quantifying the overall networkof brain regions and body parts recruited by all modules within acondition. Indeed, we can see that the togetherness strength variesacross different regions and across different conditions.

3.4 Different IBI (inter-beat interval) patternsin natural, spontaneous and deliberatewalking patterns

Given the differences in the brain-body coupled network’smodularity-based and togetherness-based profiles across conditions, and giventhe differences in the underlying stochastic signatures of the nodesacross conditions, we also examined the stochastic properties ofthe heart’s inter-beat interval (IBI) activity. We examined the vari-ability while walking with spontaneous (i.e., metronome condition)or deliberate load (i.e., paced breathing condition) in relation tonatural walking (i.e., control condition). The results are shown inFig.13 for two representative participants, including a case study ofa participant with Autism spectrum disorder (ASD), where differ-ences across conditions in the estimated PDFs and the noise levelare shown for each person. Among neurotypical participants, wefound a consistent pattern of an increase in NSR (scale/dispersion)and decrease in shape/skewness for the deliberate paced breathingcondition in relation to the natural walking (control) condition,

Figure 11: Participation matrices of togetherness amongbrain-body regions detected for each module across con-ditions for one representative participant. (A) Patterns foreach of the three modules in the normal walking condition(control). (B) Patterns for each of the two modules in the(spontaneous) metronome condition. (C) Patterns for eachof the two modules in the (deliberate) paced breathing con-dition. (D) Schematic of the matrix for Module 1 in Fig 11Afor clarity. The yellow blocks are marked as active together.They recruit the head (H), upper arms (U) including botharms and wrists, the trunk (T) and the lumbar (Lu) nodes ofthe body. Brain region coupled with these body regions isthe Prefrontal cortex (Pf). Movies of the minute-by-minuteversion of this togetherness metric across modules can beseen here.

Figure 12: Summary patterns counting the number of timesthe node of a brain or body region participated across allmodules in a session-condition. This provides a summaryof togetherness strength. Note, some body or brain regionsmay not be recruited together so they appear at 0-count.Movies of the minute-by-minute version of the summarybar-plot can be found here.

with the spontaneous metronome condition generally varying be-tween these two. This pattern was inverted for the ASD person.Overall, we can see that different families of PDFs emerged acrossthe conditions that infer profound statistical differences betweennaturally walking and walking subject to additional task loads.

In the particular case of the patient with ASD, it is noticeablethat the range of shapes in the PDFs was closer to the randomExponential limit (left of the x-axis) than to the Gaussian limit(towards the right of x-axis). Further when examining other ASDparticipants we found that the range of values of their estimatedPDF parameters were very narrow across all conditions. This isin marked contrast to controls who exhibited ample cross-talk

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MOCO ’17, 28-30 June, 2017, London, United Kingdom Ryu et al.

Figure 13: IBI stochastic profiles. (A) A representative neu-rotypical participant (B) A participant with ASD.

between the deliberate/spontaneous processes of the CNS-PNSinteractions and the inevitable heart-processes of the ANS.

4 CONCLUSIONSIn summary, we have presented a new platform and data type tostudy the coupled dynamical systems, such as the brain/CNS andthe body/PNS, during performance of natural movements. The newmethods and paradigm may serve to unify and advance the fieldsof cognitive neuroscience and neuro-motor control. They may alsobe of use to the community of performing artists as they involvecoupled interactions between different networks of the individual.

We illustrate the use of this platform and data types to integrateactivities of biophysical signals harnessed from different CNS andPNS locations, as the individual engages in the same biomechanicaltask of walking under different levels of task load. In this study,we found that simply placing a metronome in the backgroundspontaneously elicited different patterns of entrainment acrossthe brain-body networks, thus dramatically changing the networksynergies. Likewise, instructing the person to breathe at a certainpace changed the interactions in the brain-body coupled network(along with the interactions within each CNS/brain and PNS/bodynetwork).

We presented new ways to visualize self-emerging patterns thatrecruited different subnetworks during three different conditions,and quantified various levels of spontaneously arising pairwise-node coupling (self-emerging reciprocal connections) and regionalcoupling (togetherness detected in selected brain-body regions).We also presented new methods to track the evolution of the sto-chastic signatures underlying the nodes within these networks,and revealed the NSR ratio dynamically changing across differentconditions.

The dynamics of these data are best appreciated in movies thatwe included in the referenced links. However, they are also amenableto researchers performing statistical analyses on such data (e.g.,Table 1), which summarizes various statistics and parameter ranges(e.g., Fig.14) empirically determined for an individual. In fact, weused new forms of statistical inference and interpretation to por-tray an individualized profile of the participant. As such, this newplatform and data types would aid in the personalized approach em-ployed in the current medical fields (e.g. Precision Medicine and thenascent field of Precision Psychiatry). Also, this approach would sig-nificantly complement the current behavioral/observational meth-ods, which exclusively rely on subjectively acquired ordinal scales

Figure 14: Boxplot of shape and scale parameters from theestimated Gamma PDF for each condition.

and leave out the continuous flow of activities generated by themulti-layered nervous systems.

We underscore that biorhythms of the nervous systems cannow be examined in an integrated fashion across multiple lev-els of intentionality, ranging from inevitable/autonomic, to auto-matic/spontaneous, to deliberate. We hope that this multi-layeredapproach in understanding the CNS and PNS dynamic interactionswill help us advance interdisciplinary research across the computa-tional and movement fields.

ACKNOWLEDGMENTSThe study was supported by the Nancy Lurie Marks Family Foun-dation Development Career Award to EBT and the New JerseyGovernor’s Council for Research and Treatment of Autism to EBTand JSR. We thank the participants and lab members who helpedduring data collection.

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