entropy

Article
Healthcare Teams Neurodynamically Reorganize
When Resolving Uncertainty
Ronald Stevens 1,2, *, Trysha Galloway 2 , Donald Halpin 3 and Ann Willemsen-Dunlap 3
1 Brain Research Institute, University of California, Los Angeles School of Medicine,
Culver City, CA 90230, USA
2 IMMEX (Interactive Multi-Media Exercises), The Learning Chameleon, Inc., Culver City, CA 90230, USA;
trysha@teamneurodynamics.com
3 JUMP Simulation and Education Center, 1306 N Berkeley Ave, Peoria, IL 61603, USA;
donald.j.halpin@jumpsimulation.org (D.H.); ann.m.willemsen-dunlap@jumpsimulation.org (A.W.-D.)
* Correspondence: immexr@gmail.com; Tel.: +1-310-987-7863

Academic Editor: Osvaldo Anibal Rosso

Received: 23 September 2016; Accepted: 22 November 2016; Published: 29 November 2016

Abstract: Research on the microscale neural dynamics of social interactions has yet to be translated
into improvements in the assembly, training and evaluation of teams. This is partially due to the scale
of neural involvements in team activities, spanning the millisecond oscillations in individual brains
to the minutes/hours performance behaviors of the team. We have used intermediate neurodynamic
representations to show that healthcare teams enter persistent (50100 s) neurodynamic states
when they encounter and resolve uncertainty while managing simulated patients. Each of the
second symbols was developed situating the electroencephalogram (EEG) power of each team
member in the contexts of those of other team members and the task. These representations were
acquired from EEG headsets with 19 recording electrodes for each of the 140 Hz frequencies.
Estimates of the information in each symbol stream were calculated from a 60 s moving window
of Shannon entropy that was updated each second, providing a quantitative neurodynamic history
of the teams performance. Neurodynamic organizations fluctuated with the task demands with
increased organization (i.e., lower entropy) occurring when the team needed to resolve uncertainty.
These results show that intermediate neurodynamic representations can provide a quantitative bridge
between the micro and macro scales of teamwork.

Keywords: team neurodynamics; Shannon entropy; EEG; teamwork; healthcare; uncertainty

1. Introduction

1.1. Background
Teams work through coordinated exchanges of information using speech [1], action-understandings
like gestures [2,3], posture [4], facial expressions [5], other non-verbal communications [6], and even
periods of silence [7], all of which contribute to the teams dynamics. It is not surprising that
neurophysiologic processes underlie these interactions, and, while research is revealing the microscale
details of social dynamics [8], the impact of these studies on understanding how to assemble, train and
evaluate teams has been minor. This is partially due to the time span of neural involvements in team
activities, ranging from the millisecond neurodynamic oscillations in individual brains to the observed
performance behaviors in the overall team that occur over hours/days.
The powerlaw structures of the data streams left by individuals at both the neuronal level

(10 10 s) [9,10] as well as processes left by spontaneous (100105 s) human behavior [11,12] and
3

teamwork (i.e., speech) [13], however, suggests that points may exist along this 108 s time scale,

Entropy 2016, 18, 427; doi:10.3390/e18120427 www.mdpi.com/journal/entropy

Entropy 2016, 18, 427 2 of 15

where intermediate representations could capture the micro-neurodynamics and transform them into
other representations that link to higher level team behaviors [14]. In these representations, what would
be lost in the mechanistic details of neuronal spike generation and propagation would be gained by
tighter relationships with more easily-recognized, observer-defined variables such as team coherence,
flexibility or resilience.
Several years ago, we explored an information/organization-centric approach for developing
transitional neurodynamic representations with the goal of quantitatively mapping the
neurophysiologic organizations of teams and relating their fluctuating dynamics to team activities,
communications, and performance [15,16].
Long-term, the benefits of such quantitative models of teamwork, if appropriately positioned
along the micromacro continuum of teamwork, would include the ability to compare across
teams, or training sites, or training protocols, and to follow team training progress over time.
Reiteratively, if appropriately positioned below the domain specificity of complex tasks, but above the
100300 millisecond timings of responses like imitation and action perception [17], these modeling
approaches would be applicable to many complex teaming situations.
We accomplished these goals with measures that were rapid yet encompassed many facets of
cognition. Electroencephalography (EEG) was chosen for these studies as it provided real-time and
high resolution temporal recording of the brains electrical activity of an alternating type at different
regions along the scalp and at different frequencies measured in an unobtrusive fashion.

1.2. Neurodynamic Modeling

The goal of the neurodynamic modeling was to develop data streams that contained temporal
information about the organization, function and performance of teams. The first step in the
neurodynamic modeling was to generate Neurodynamic Symbols (NS), which are symbolic
representations of the momentary power levels of a neurodynamic marker for each team member.
Every second, the power levels of one of the EEG frequencies (i.e., 40 Hz) bins of each of the three team
members were compared to his/her own task balance levels. This identified whether at a particular
time point a person was experiencing above or below average levels of an EEG marker, and also
showed whether the team as a whole was experiencing above or below average levels.
In this study, we highlight the 10 Hz frequency, which is involved in attention and prioritizing
stimuli [18,19], the 16 Hz frequency that is involved in action understandings [17], and the
40 Hz frequency involved in maintaining working memory and long-term memory encoding and
retrieval [20,21]. The frequencies that were chosen for this study were based on prior work that
revealed their involvement in team neurodynamics [16,22].
It is important to note that, functionally, high and low EEG power in these frequency bands should
not be thought of as good or bad, as different power levels may serve different purposes. For instance,
during spontaneous coordination, the mu medial rhythm is synchronized (i.e., high power),
but becomes suppressed or desynchronized (i.e., low power) during social interaction [8]. Similarly,
synchronized (i.e., high power) alpha may provide a mechanism for selective attention while
desynchronized alpha may promote working memory formation [19].
During neurodynamic modeling, the frequency-specific EEG power levels become partitioned
into the upper 33%, the lower 33% and the middle 33%, which were assigned values of 3, 1, and 1,
respectively, and these values were chosen for data visualization purposes. Each second, the values
for each person were combined into a three-element vector. The values for the three histograms in
Figure 1A indicate that, at this point in time, team member 1 had below average frequency-specific
EEG power levels, team member 2 had above average, and team member 3 had average levels, and so
the vector for this neurodynamic symbol (NS) would be 1, 3, 1. The three element vectors created
each second for the performance were classified by unsupervised artificial neural networks to create
a twenty-one symbol neurodynamic state space (NSS) (Figure 1B).
Entropy 2016, 18, 427 3 of 15

Entropy In2016,
the 18,
process
427 of developing the NSS, a topology was generated such that the early symbols 3 of 15
(numbered row wise 15, 610, etc.) represented times when most team members had average/low
levels of EEG power, while the symbols on the bottom row, numbers 2025 represented times when
most team members had above average power levels. Each NS in the symbolic state space therefore
situated the EEG power levels of each team member in the context of the levels of the other team
members. Classifying
Classifying the the set
set of
of symbols
symbols overover entire
entire performances
performances (i.e., Briefing, Scenario and
Debriefing segments) provided neurodynamic neurodynamic models models encompassing
encompassing aa comprehensive
comprehensive set set of task
situations/loads
situations/loads [23]. [23].
The hypothesis was that brain-wide collections collections of such sequences
sequences would
would contain
contain second-by-
second-by-
second neurodynamic
neurodynamichistories historiesofofthethe
team, where
team, the information
where the informationcontained in each
contained insecond would
each second
dependdepend
would on theonEEG the EEG frequencies
frequencies andand channels
channelsbeing
beinganalyzed.
analyzed. Second-by-second
Second-by-second symbolic
representations were were developed
developedthat thatshowed
showedthe theEEGEEGpower
power levels over
levels overthethe
140 Hz Hz
140 spectrum
spectrumfor
each
for each teamteammember
member in relation to those
in relation of other
to those teamteam
of other members
membersfor the
for entire performance.
the entire performance.The
fluctuating
The information
fluctuating information in these symbol
in these streams
symbol wouldwould
streams then bethen
quantitated using a regularly
be quantitated updated
using a regularly
(i.e.,
updated each(i.e.,
second),
each 60 s sliding
second), 60 window
s sliding of Shannons
window entropy [22,24];
of Shannons entropythe quantitative
[22,24]; output measure
the quantitative output
on the y-axis would be the neurodynamic entropy measured in information
measure on the y-axis would be the neurodynamic entropy measured in information bits. bits.
In this process, the millisecond frequency-specific EEG power levels become transformed into
quantitative information about the teams neurodynamic organization. Performance segments with
restricted symbol expression had lower NSH H levels,
levels, which
which may
may reflect
reflect rigidity, while segments with
greater symbol diversity had higher entropy, entropy, which
whichmaymayreflect
reflectneurodynamic
neurodynamicflexibility.
flexibility.

Figure 1.
Figure Neurodynamic symbols
1. Neurodynamic symbols and
and symbol
symbol space.
space. (A)
(A) sample
sample neurodynamic
neurodynamic symbol
symbol (NS)
(NS) showing
showing
the power
the power levels
levels of
of three
three team
team members;
members; (B)
(B) the
the twenty-one
twenty-one symbol
symbol state
state space
space (NSS)
(NSS) that
that was
was used
used
for creating the neurodynamic symbol data streams; and (C) the frequencies of the twenty-one
for creating the neurodynamic symbol data streams; and (C) the frequencies of the twenty-one symbols
at the 40 at
symbols Hzthefrequency from the from
40 Hz frequency C4 channel
the C4for one performance.
channel for one performance.

This hypothesis was tested with US Navy submarine navigation teams performing required
training simulations
simulations[16,25].
[16,25].The
Theneurodynamic
neurodynamic symbol
symbol entropy
entropy (abbreviated
(abbreviated NSHNS H) profile
) profile of oneofteam
one
team (Figure
(Figure 2) was2)irregular
was irregular with fluctuations
with fluctuations occurring
occurring in the
in the three three training
training segments. segments.
Midway Midway
through
through the Scenario,
the Scenario, this teamthis
wasteam was challenged
challenged by fog,
by fog, heavy heavy currents
currents and multiple
and multiple other ships other ships
in the in
area
the area
while while
they they navigated
navigated through athrough
narrow astretch
narrow of stretch of water.
water. From ~2000 From ~2000
to 2700 s, to 2700
there wass, there
danger was
of
danger of collision with another ship. During this time, the NS dropped, indicating
collision with another ship. During this time, the NSH dropped, indicating a change in the level of
H a change in the
level of neurodynamic
neurodynamic organization
organization of the
of the team. team. Decreased
Decreased NSH indicates
NSH indicates that fewer that
of fewer of the available
the available symbols
symbols
were were expressed
expressed during theduring
slidingthe sliding of
window window of time, generally
time, generally 60 s or 10060s sdepending
or 100 s depending on the
on the length of
length of the performance. Further studies showed that these entropy profiles were
the performance. Further studies showed that these entropy profiles were multifractal [26] with highly multifractal [26]
with highly
dynamic, dynamic,
complex flowscomplex flows of neurodynamic
of neurodynamic information
information occurring occurring
across the teamacross the team
in response in
to the
response
changing to thedemands;
task changingthese
task dynamics
demands;were theseparticularly
dynamics were particularly
increased increased
during periods of during
apparent periods
stress.
of apparent stress.
Entropy 2016, 18, 427 4 of 15
Entropy 2016, 18, 427 4 of 15

Figure 2. Neurodynamic
Figure 2. Neurodynamic entropy
entropy profile.
profile. Neurodynamic
Neurodynamic entropy
entropy profile
profile for
for aa submarine
submarine navigation
navigation
team highlighting the major task segments (i.e., the Briefing, Scenario and Debriefing
team highlighting the major task segments (i.e., the Briefing, Scenario and Debriefing segments), as well
segments), as
as a period
well during
as a period the Scenario
during whenwhen
the Scenario the submarine almost
the submarine collided
almost with another
collided vessel.
with another vessel.

Modeling continuous
Modeling continuous EEGEEGdatadata streams
streams with performing
with teams teams performing realistic simulations
realistic simulations is challenging. is
challenging.
Scalp EEG is Scalp
thoughtEEG toisarise
thought
fromtonear-synchronous
arise from near-synchronous
field activitiesfield activities
within smallwithin
corticalsmall cortical
regions or
regions orthat
patches patches that are
are detected bydetected
EEG sensors by EEG
[27].sensors
These [27].
rhythmsThesearerhythms are also
also volume volume as
conducted conducted
far-field
as far-field
signals signals
to other EEGtosensors,
other EEG sensors,
becoming becoming
a mix a mix
of signals of signals ofand
of within-brain within-brain
non-brain and non-brain
contaminating
contaminating
signals. signals. environments,
In real-world In real-world environments,
subjects frequently subjects frequently
generate generate
ocular, facial andocular,
other facial and
muscle
other muscle
artifacts (EMG), artifacts
which (EMG), whichhighest
are generally are generally highestfrequency
in the gamma in the gamma regionfrequency
(>35 Hz) with region less(>35 Hz)
activity
with
in theless
betaactivity
(1525 in Hz)theand
beta (1525
alpha Hz)Hz)
(812 and alpha [28].
regions (812The Hz)EMGregionsnoise[28]. The EMG
is lowest alongnoisetheismidline,
lowest
alongFCz,
e.g., the midline,
Cz and CPz e.g., FCz, Cz and
channels andCPz channels
greatest alongandthegreatest
sides along
of thethe sides
head, of the
e.g., FC3, head,
FC4,e.g.,C5 FC3,
and
FC4,
C6 C5 and C6
channels. Anchannels.
importantAn important consideration
consideration for the detection for the detection
of the of the most team
most informative informative
dynamics teamis
dynamics
the optimum is the optimum
selection selection and representation
and representation of the EEG sensors of theandEEG sensors and
frequencies. frequencies.
Despite Despite
these challenges,
these
our challenges,
prior our priorthat
results suggested results suggested
entropic measures that
of entropic
frequencymeasures of frequencysymbol
specific EEG-derived specific EEG-
streams
derived
might symbol
provide streams
a way might provide
of quantitatively a way the
monitoring of quantitatively
neurodynamic monitoring
organizations theof neurodynamic
teams.
organizations of teams.
The first research question for this study was: Are the neurodynamic organizations of teams
uniqueThetofirst research
submarine question teams,
navigation for thisorstudy
are theywas: Arefundamental
more the neurodynamic propertiesorganizations of teams
of teams performing
unique
in to submarine
complex environments?navigation
In thisteams,
study,orwearehave
theytested
more fundamental
this hypothesis properties of teamsteams.
with healthcare performing
in complex
The secondenvironments? In this study,
research question we have
was: What is thetested this hypothesis
behavioral significance with healthcare
of these teams. level
intermediate
The secondfluctuations?
neurodynamic research questionEarlier was:
workWhatwithis the behavioral
submarine significance
navigation of these
teams intermediate
suggested level
that entropy
neurodynamic
decreases mightfluctuations?
be associatedEarlier work with
with periods submarine
of stress and/or navigation
uncertainty.teams suggested that
The three-member entropy
healthcare
decreases
teams includedmight be associated
in this study (rather with
thanperiods of stresssubmarine
the 56 member and/or uncertainty.
teams) allowed Thea three-member
more detailed
healthcareofteams
mapping included in this activities
the second-by-second study (rather than
of each teamthemember
56 member to beginsubmarine
to approach teams)thisallowed
question. a
more detailed mapping of the second-by-second activities of each team
These detailed activity mappings also help address the question of whether the entropy fluctuationsmember to begin to approach
this question.
were the directThese
resultdetailed activity
of excessive EMG mappings
activity.also help address the question of whether the entropy
fluctuations were the direct result of excessive EMG activity.
2. Materials and Methods
2. Materials and Methods
2.1. Simulations
2.1. Simulations
The simulations developed for this study followed a standard training format beginning with
a pre-simulation
The simulationsbriefing of approximately
developed ten minutes.
for this study followedThis orientation
a standard focused
training on establishing
format a safea
beginning with
learning environment and provided an introduction to the simulated clinical setting, the
pre-simulation briefing of approximately ten minutes. This orientation focused on establishing a safe equipment and
supplies, the mannequin,
learning environment asprovided
and well as anan
overview of what
introduction totothe
expect duringclinical
simulated the postsetting,
simulation debriefing.
the equipment
Teams were briefed on key roles needed to manage a patient with an urgent/emergent
and supplies, the mannequin, as well as an overview of what to expect during the post simulation clinical
condition; these included: Leadership, Compressions, a Scribe, Airway/Breathing,
debriefing. Teams were briefed on key roles needed to manage a patient with an urgent/emergent Medication/Fluid
Administration,
clinical condition; Electrical
these Therapy,
included:Pulses and Monitors.
Leadership, This was followed
Compressions, by a Airway/Breathing,
a Scribe, short introduction
including the simulated patient history and set the stage for the simulation. The
Medication/Fluid Administration, Electrical Therapy, Pulses and Monitors. This was followed briefing was followed
by a
by the simulation scenario lasting 15 20 min. A reflective debriefing was then
short introduction including the simulated patient history and set the stage for the simulation.led by the instructor
The
(15 20 min)
briefing was [29].
followed by the simulation scenario lasting 1520 min. A reflective debriefing was then
led by the instructor (1520 min) [29].
Entropy 2016, 18, 427 5 of 15

The core construct of this simulation series was ventilation with procedural goals of demonstrating
the technical skills of supporting the airway of an obtunded patient and cognitive goals of carrying
out team-based approaches to patients with decreased mental status, as well as practicing role
assignment during care of a patient with an urgent/emergent clinical condition and the discussion of
contraindications for Flumazenil-reversal of benzodiazepine (BZD) induced respiratory depression.
Benzodiazepines are a commonly prescribed family of depressants that are often used to treat general
anxiety, insomnia, depression, panic disorders, seizures and acute stress reactions. This construct was
presented to the medical students with a simulated patient found unresponsive in his apartment and
transported by Emergency Medical Services to the Emergency Department. The patient was obtunded
due to a likely Benzodiazepine overdose and required supportive management. The construct design
included the induction (depending on the sequence of team actions) of Benzodiazepine withdrawal
syndrome which is a cluster of symptoms that emerge when a person who has taken Benzodiazepine,
either medically or recreationally, and has developed a physical dependence, undergoes dosage
reduction or discontinuation. This study reports the dynamics of five teams who have performed
this or similar healthcare simulations. The study was approved for human use by the Order of Saint
Francis IRB and all team performances were rated by experienced TeamSTEPPS raters [29].
The submarine navigation studies referenced for this study (n = 7) averaged 4676 s in length with
a range of 40205298 s. The healthcare simulations (n = 11) were shorter, averaging 1787 s with a range
of 10812534 s. Combined, this represented over 14 h of teamwork.

2.2. Electroencephalography
EEG data was collected using the Quick 20 EEG headset from Cognionics, Inc. (Carlsbad,
CA, USA), with 19 recording electrodes in the international 1020 position with reference on A1,
placing channel locations at F7, Fp1, Fp2, F8, F3, Fz, F4, C3, Cz, P8, P7, Pz, P4, T3, P3, O1, O2,
C4, T4 monopolar configuration grounded to linked earlobes. The sampling frequency was 500 Hz.
EEG data were preprocessed for each team member using FieldTrip (Donders Institute for Brain,
Cognition and Behaviour, Nijmegen, NL) [30] by applying high-pass (0.5 Hz) and low-pass filters
(50 Hz) and removing bad channels (max = 2). Spatially transformed independent component
analysis was performed with RUNICA [31] to detect and remove artifacts associated with eye blinks,
electrocardiogram and electromyogram activity. Following artifact rejection using RUNICA, data were
back-reconstructed, and channels removed prior to RUNICA decomposition were interpolated back
into the data by spherical interpolation.
Frequency decomposition was performed by first segmenting data into 1 s epochs. The EEG data
were then windowed into 1 s epochs using Hanning taper and the frequency content of each trial was
measured at 1 Hz intervals from 140 Hz using Fast Fourier Transform.

3. Results

3.1. Neurodynamic Fluctuations at Different Sensor Channels

For the current studies, 19 sensor headsets (Cognionics Quick 20, Carlsbad, CA, USA) were
available, which allowed us to achieve a finer level of analysis than that afforded by nine sensor
headsets in previous studies. With forty 1 Hz frequency bins in each channel, there were
760 frequencydata streams for analysis. To simplify analysis and interpretation of the data, we explored
ways of reducing this dimensionality while maintaining core dynamic features of the neurodynamic
models. As a prelude to studying the teams neurodynamic responses, the initial studies first surveyed
the frequency profile of the neurodynamic entropy expression over the 140 Hz EEG frequency range
(Figure 3A), and this was followed by correlation studies among the different frequency bands to detect
redundancies and possible cross-frequency interactions (Figure 3B). This was followed by an across
scalp survey to determine the sensors with the maximum/minimum neurodynamic entropy levels,
as well as possible cross-sensor interactions (Figure 3C).
Entropy 2016, 18, 427 6 of 15
Entropy 2016, 18, 427 6 of 15

Previous studies
Previous studieswithwithsubmarine
submarinenavigation
navigation and and high
high school
school problem
problem solving
solving teams teams showed
showed few
few apparent
apparent team neurodynamic
team neurodynamic organizations
organizations in the
in the delta (23delta
Hz) (23 Hz)(46
or theta or theta (46 Hz)
Hz) bands, bands,
suggesting
suggesting
that that of
the number thefrequencies
number oftofrequencies
be analyzedtomightbe analyzed
be reduced might be reduced
to the alpha (812 to the
Hz),alpha (812 Hz),
beta (1625 Hz)
beta gamma
and (1625 Hz)(32 and gamma
Hz and (32 Hz
higher) and higher)
bands. Based on bands. Based on the
the harmonic harmonic relationships
relationships of these
of these frequencies,
frequencies,distinction
maximum maximumbetween distinction between
these bandsthese
could bands could beby
be achieved achieved
selecting by the
selecting
10 Hz,the 1610HzHz, 16
and
Hz and 3540 Hz frequencies for the initial healthcare studies [19]. As facial
3540 Hz frequencies for the initial healthcare studies [19]. As facial EMG noise begin to predominate EMG noise begin to
predominate
at above 40 Hz,atthisabove 40 Hz,
frequency thiswould
range frequency
also berange
usefulwould also be useful
for investigating for investigating
the contribution of EMGthe to
contribution of EMG
the NSH fluctuations. to the NS H fluctuations.
The average
The averageNS NSHHlevels
levelsofofthe
thenineteen
nineteen sensor
sensor arrays
arrays areare plotted
plotted for for
the the
fortyforty
1 Hz1frequency
Hz frequencybins
bins
in in Figure
Figure 3A. From
3A. From this profile,
this profile, we wouldwe would
expectexpect the magnitude,
the magnitude, frequency
frequency and/orand/or durations
durations of
of the
the NS fluctuations for healthcare teams would be greatest for the 40 Hz profile,
NSH fluctuations for healthcare teams would be greatest for the 40 Hz profile, less for 16 Hz, and least
H less for 16 Hz, and
least
for 10for 10 Figure
Hz. Hz. Figure 3B shows
3B shows the the frequency
frequency x frequency
frequency correlation
correlation values
values forNS
for NSHH . .The
The correlation
correlation
between the
between the levels
levels ofof alpha
alpha and
and gamma
gamma NS NSHH from five different
different teams
teams was
was lowlow toto negative,
negative, while
while the
the
correlations of the beta bands and the alpha and gamma bands were more
correlations of the beta bands and the alpha and gamma bands were more moderate (r = 0.450.58). moderate (r = 0.450.58).

Figure 3.
Figure 3. NS Entropy levels for different electroencephalographic (EEG) frequencies and sensors.
(A) The
(A) The average
average NS NS entropy
entropy for
for the
the nineteen
nineteen EEG
EEG sensors
sensors isis plotted
plotted vs.
vs. the EEG frequency;
(B) Neurodynamic entropy
(B) Neurodynamic entropy (NSH (NS H ) correlations across different frequency bands.
across different frequency bands. These These correlations
correlations
weremade
were madefromfrom five
five teamteam performances;
performances; andthe
and (C) (C)NSthe NSH correlations
H correlations across
across the EEGthe EEGmontage
sensors sensors
montage
for for one
one team. Theteam. Theare
sensors sensors
in theare in the
order: order:
F7, Fp1, F7,
Fp2,Fp1,
F8, Fp2, F8,F4,
F3, Fz, F3,C3,
Fz, Cz,
F4, C3,
C4, Cz, C4, P4,
P8, Pz, P8, T3,
Pz, T4,
P4,
T3, T4,
O1, O2.O1,
TheO2. The P7 was
P7 sensor sensor
notwas not included
included in the analyses
in the analyses for technical
for technical reasons.reasons.

The decision
The decisionasastoto which
which sensors
sensors to highlight
to highlight in theinmodeling
the modeling
was less was less
clear fromclear from
both both the
the literature
literature
and and prior experiments
prior experiments as the brain as the brain
topologies of topologies
the EEG power of the EEG power
contributing to contributing to team
team neurodynamics
are unknown at this time. To estimate the contributions of different sensors to the performancetoNS
neurodynamics are unknown at this time. To estimate the contributions of different sensors the,
H
performancewere
correlations NSH, made
correlations
across were
the 18made across
sensors usingthe the
18 sensors usingwhich
NSH levels, the NSwere
H levels, which were the
the average of the
average
40 one Hz offrequency
the 40 onebins.
Hz frequency bins.
In Figure 3C, the sensors were
In Figure 3C, the sensors were ordered
ordered for for the
the Frontal
Frontal (F)
(F) groups
groups (F7,
(F7, Fp1,
Fp1, Fp2,
Fp2, F8,
F8, F3,
F3, Fz,
Fz, F4),
F4),
for the
for the Central
Central (C)
(C) group
group (C3,
(C3, Cz,
Cz, C4),
C4), the
the Parietal
Parietal (P)
(P) group
group (P8,
(P8, Pz,
Pz, P4,
P4, P3),
P3), the
the Temporal
Temporal (T)(T) group
group
(T3, T4) and the Occipital (O) group (O1, O2). Most of the correlations were high,
(T3, T4) and the Occipital (O) group (O1, O2). Most of the correlations were high, ranging from r = 0.7 ranging from r=
0.7 to 0.9 with the exception of the Occipital group, where the correlations with non-occipital
to 0.9 with the exception of the Occipital group, where the correlations with non-occipital sensors were sensors
were
as lowasaslow
r = as r = 0.45.
0.45.
The correlation studies for
The correlation studies for the
the EEG
EEG sensors
sensors were
were followed
followed byby plotting
plotting the
the temporal
temporalNS NSH profiles
profiles
H
for these
for these sensor
sensor series
series arranged
arranged fromfrom the
the anterior
anterior toto the
the posterior
posterior of of the
the scalp.
scalp. These
These entropy
entropy profiles
profiles
used the average NS H dynamics of the 140 Hz frequency spectrum (Figure 4).
used the average NSH dynamics of the 140 Hz frequency spectrum (Figure 4).
The NSNSH profiles for the five sensor series were qualitatively similar with NSH decreases ~380 s,
The H profiles for the five sensor series were qualitatively similar with NSH decreases ~380 s,
650 s,
650 s, 960
960 ss and
and 1100
1100 ss (Figure
(Figure 4A).
4A). The
The largest
largest quantitative
quantitative differences
differences were
were seen
seen with
with the
the O-sensor
O-sensor
series which were highest during the Debriefing segment (>800 s). An across-frequency
series which were highest during the Debriefing segment (>800 s). An across-frequency and time and time plot
plot
(Figure 4B) was made of the NSH for the O-series, which showed that much of the decreased NSH
activity in the Debriefing segment was across the ~1240 Hz bands.
Entropy 2016, 18, 427 7 of 15

(Figure 4B) was made of the NSH for the O-series, which showed that much of the decreased NSH
activity2016,
Entropy in the Debriefing
18, 427 segment was across the ~1240 Hz bands. 7 of 15

Figure 4. Neurodynamic
Figure 4. Neurodynamic entropy
entropy profiles
profiles for
for EEG
EEG sensor
sensor series
series during
during one
one healthcare
healthcare simulation.
simulation.
(A)
(A) Average
Average 140
140 Hz
Hz NS
NSHH dynamics
dynamics for
for series
series of
of different
different EEG
EEG sensors.
sensors. The
The F-series
F-series shows
shows the
the average
average
NS
NS entropy
entropy for
for the
the Fp2,
Fp2, F8,
F8, F4,
F4, Fz,
Fz, F3,
F3, F7
F7 and
and FP1
FP1 channels.
channels. The
The C-series
C-series were
were averaged
averaged from
from the
the C3,
C3,
Cz and C4 channel sites. The P-series were averaged from the P3, Pz, P4, P5 sensors and
Cz and C4 channel sites. The P-series were averaged from the P3, Pz, P4, P5 sensors and the O-series the O-series
were from the
were from the averaged
averaged from
from the
the O1
O1 and
and O2
O2 channels;
channels; and
and (B)
(B) across-frequency
across-frequency plot
plot of
of the
the NS
NSHH from
from
the
the O-series
O-series channels.
channels.

3.2.
3.2. FrequencyEntropy
FrequencyEntropy Differences
Differences
For
For studying
studying the detailed across-frequency
the detailed across-frequency and and across-activity
across-activity teamteam dynamics,
dynamics, we we chose
chose toto
analyze the 10 Hz, 16 Hz and 40 Hz frequencies from the C4 sensor.
analyze the 10 Hz, 16 Hz and 40 Hz frequencies from the C4 sensor. These sensorfrequency These sensorfrequency
combinations
combinations should
should provide
provide information
information regarding
regarding thethe similarity
similarity between
between healthcare
healthcare teams
teams andand
submarine navigation teams (where 10 Hz and 40 Hz entropy decreases
submarine navigation teams (where 10 Hz and 40 Hz entropy decreases predominated), and high predominated), and high
school
school map
map navigation
navigation teams
teams (where
(where entropy
entropy fluctuations
fluctuations were
were mainly
mainly at at the
the 16
16 Hz
Hz and
and 40 40 Hz
Hz
frequencies). The C4 scalp position should also reveal significant EMG contributions
frequencies). The C4 scalp position should also reveal significant EMG contributions to entropy to entropy
fluctuations
fluctuations ifif they
they were present [28].
were present [28].
The NS H profiles for one team (J10T2) at the 40 Hz, 16 Hz and 10 Hz frequencies (of the C4 sensor)
The NSH profiles for one team (J10T2) at the 40 Hz, 16 Hz and 10 Hz frequencies (of the C4 sensor)
are
are shown in
shown in Figure 5. There
Figure 5. There were multiple episodes
were multiple episodes of of decreased
decreased NS NSH in the three frequency bands
H in the three frequency bands
with
with the most prominent presented in the 40 Hz frequency band (FigureAs
the most prominent presented in the 40 Hz frequency band (Figure 5A). expected
5A). from Figure
As expected from
3B, the 3B,
Figure overlap of the decreased
the overlap NSH segments
of the decreased in the different
NSH segments profilesprofiles
in the different was low.was low.
The
The maximum
maximumentropyentropyfromfrom2121symbols
symbols that areare
that randomly
randomly distributed
distributedin the datadata
in the stream is 4.39
stream is
bits.
4.39 bits. The maximum entropy across the 140 Hz frequency bins for the C4 channel was (~20
The maximum entropy across the 140 Hz frequency bins for the C4 channel was 4.31 4.31
symbols), suggesting
(~20 symbols), that the
suggesting symbols
that were not
the symbols wererandomly represented
not randomly within the
represented datathe
within stream
data (Figure
stream
1C). The minimum entropy (above the 5 Hz frequency) was 3.2 (or ~9 of the
(Figure 1C). The minimum entropy (above the 5 Hz frequency) was 3.2 (or ~9 of the 21 symbols) 21 symbols) over a over
60 s
moving window, i.e., about 50% of the available neurodynamic
a 60 s moving window, i.e., about 50% of the available neurodynamic states. states.
Entropy 2016, 18, 427 8 of 15
Entropy 2016, 18, 427 8 of 15

Figure 5.
Figure NSHH profiles
5. NS profilesat
at (A)
(A) 40
40 Hz;
Hz; (B)
(B) 16
16 Hz
Hz and
and (C)
(C) 10
10 Hz.
Hz. These
These profiles
profiles were
were from
from the
the C4
C4 sensor
sensor
and is the same data set used for Figure
and is the same data set used for Figure 7. 7.

The
The NS NSHHprofiles
profilesin
inFigures
Figures 44andand55indicated
indicatedthatthatthere
therewere
wereintersegment
intersegment (i.e.,
(i.e., Briefing,
Briefing, Scenario
Scenario
and Debriefing), as well as intra-segment regions of increased symbol organization.
and Debriefing), as well as intra-segment regions of increased symbol organization. In this paper, In this paper, we
highlight
we highlight the the
changes
changesin the
in theneurodynamic
neurodynamic entropy
entropy levels
levelsthat
thatare
areshown
shownby bythetheline
line traces.
traces. ItIt is
is
important to note, however, that there is useful information in the symbols themselves
important to note, however, that there is useful information in the symbols themselves that relates to the that relates to
the overall
overall EEG EEGpowerpower
levels levels of the different
of the different membersmembers
of the team. of These
the team. These relationships
relationships can be visualized can be by
visualized
plotting theby plottingorder
temporal the temporal order ofofeach
of each symbol the symbol
NS sequenceof theofNS sequence of a(Figure
a performance performance6). This(Figure
figure
6). This
plots thefigure plots the
occurrence of occurrence
each of theof 21each of theduring
symbols 21 symbols during the performance,
the performance, and shows that and the
shows that
symbol
the symbol isexpression
expression not random,is not
butrandom, but is by
is punctuated punctuated
periods whereby periods
sets ofwhere
symbols sets
areofmore
symbols are more
frequent than
frequent
others. The than others. The
dominant dominant
symbols during symbols during
five of these five ofare
periods these periodsaround
expanded are expanded
the central around
figure. the
central figure.
One feature of these symbol groupings was that the symbols in each group were mostly contiguous.
This One feature
indicates thatofchanges
these symbolin the groupings was that the
power relationships symbols
across the teamin each
were group were mostly
small during these
contiguous. This indicates that changes in the power relationships across
persistent states, reminiscent of attractor states seen with the submarine navigation teams [25].the team were small during
theseApersistent states, reminiscent
second feature was that theofgroupings
attractor states seen with
consisted the submarine
of periods where all navigation
team members teams [25].
had
highA40second featurelevels,
Hz power was that or the groupings
periods where consisted
all had oflowperiods
power, where all team members
or periods had high
with intermediate
40 Hz power
power levels levels,
acrossor periods
the team. where all had low
For instance, power,
during the or periodsand
Briefing with intermediate
Debriefing power levels
segments, NS 1,
across the team. For instance, during the Briefing and Debriefing
3, and 4 predominated, representing periods where most of the team members had below segments, NS 1, 3,average
and 4
predominated,
40 Hz EEG power. representing periods where
The NS expressions in themost of the team
Scenario were members
more variablehad below
with NS average
202440 Hz EEG
associated
power. The NS expressions in the Scenario were more
with episode 1, NS 1417 with episode 2 and NS 2325 with episode 3. variable with NS 2024 associated with episode
1, NS 1417 with episode 2 and NS 2325 with episode 3.
Entropy 2016, 18, 427 9 of 15
Entropy 2016, 18, 427 9 of 15

Figure
Figure 6.
6. Symbol
Symbol distributions
distributions associated
associated with
with major
major entropy
entropy fluctuations
fluctuations at
at 40
40 Hz.
Hz. (A)
(A) The
The second-
second-
by-second
by-second expressions of each of the NS are shown for the period of the performance; (B) The symbols
expressions of each of the NS are shown for the period of the performance; (B) The symbols
expressed
expressed during
during periods of low
periods of low NS
NSH H are
are highlighted
highlighted around
around the
the expression
expression map.
map.

3.3.
3.3. NS
NSHH Decreases
DecreasesReflect
Reflect Teams
Teams in
in the
the Process
Process of
of Resolving
Resolving Uncertainty
Uncertainty
The
The next series of
next series of analyses
analyses linked
linked NS NSH changes
changes withwith different
different activities/actions
activities/actions of of the
the team;
team;
H
Episodes
Episodes 1, 2 and 3 are highlighted in these studies (Figure 7). The first episode of the 40
1, 2 and 3 are highlighted in these studies (Figure 7). The first episode of the 40 HzHz
neurodynamic
neurodynamic entropy entropy decrease
decrease (215315
(215315 s), s), Figure
Figure 7A,7A, started
started when
when the the patient
patient vomited
vomited (~212(~212 s) s)
initiating a planning discussion among the team members. Suction
initiating a planning discussion among the team members. Suction was started while the team decided was started while the team
decided to: (a) administer
to: (a) administer Flumazenil; Flumazenil; (b) and
(b) start fluids start(c)fluids
deliverand (c) deliver
oxygen. oxygen.
Flumazenil is aFlumazenil
benzodiazepine is a
benzodiazepine receptor antagonist which competes with benzodiazepine
receptor antagonist which competes with benzodiazepine for the receptor and reverses the effects for the receptor and
of
reverses the effects
benzodiazepine. The of40
benzodiazepine.
Hz NSH of the team The 40 Hz NSH ofdropped
continually the teamduring
continually dropped during these
these discussions/decisions,
discussions/decisions,
and began to rise afterand the began to risewas
Flumazenil after the Flumazenil
administered was administered
and fluids were flowing; and fluids
a few were
seconds
flowing;
later, the aoxygen
few seconds later, the
was started. Theoxygen was started.
team began evaluating Thetheteam began
effects evaluating
of their the effects
interventions of their
as the NSH
interventions as the NS H reached earlier levels; the episode lasted 100 s.
reached earlier levels; the episode lasted 100 s.
The
The neurodynamic
neurodynamic organizations
organizations responsible
responsible for for the
the decreased
decreased entropy
entropy were were determined
determined from from
Figure 6 (Episode 1), and most of the team members had high
Figure 6 (Episode 1), and most of the team members had high 40 Hz EEG power while NSH was 40 Hz EEG power while NS H was

dropping
dropping and and as NSH rose
as NS the 40 Hz power generally decreased.
H rose the 40 Hz power generally decreased.
The second episode
The second episode of decliningof declining 40 NS
40 Hz Hz NS H began ~340 s when the patient started having
H began ~340 s when the patient started having seizures
seizures
as a resultasofa the
result of the Flumazenil
Flumazenil administration
administration (Figure 7B). (Figure 7B). The
The team teamthat
realized realized that the
the patient may patient
have
may have been chronically taking benzodiazepine and was entering
been chronically taking benzodiazepine and was entering withdrawal due to receptor blockage by withdrawal due to receptor
blockage
Flumazenil. by At Flumazenil.
396 s, TeamAt 396 s, 2Team
Member stated:Member 2 stated: [benzo]
Get something Get something
on board if[benzo]
hes . . .on board if
chronically
heschronically
taking it, we just took taking it, away
it all we justfromtook it allThe
him. awayNSH from
beganhim. TheasNS
rising theH began rising as
team decided tothe team
intubate
decided to intubate to maximize ventilation while they searched
to maximize ventilation while they searched for Ativan. While Team Member 2 was leading the for Ativan. While Team Member 2
was leadingregarding
discussion the discussion regarding withdrawal,
benzodiazepine benzodiazepine the NSwithdrawal, the NSH was dropping, and his 40
H was dropping, and his 40 Hz power levels
Hz
were high (NS #16 and #17 in Figure 6). Once the team decision wasdecision
power levels were high (NS #16 and #17 in Figure 6). Once the team made towas made the
intubate to intubate
patient
the
(~400 s), Team Member 2s 40 Hz power levels decreased and remained low, even during the during
patient (~400 s), Team Member 2s 40 Hz power levels decreased and remained low, even period
the
from period
435 tofrom450 s435whento 450
he wass when he was vigorously
vigorously pumping up pumping
the bed upwith thehis
bed with
right leghis
to right
raise leg
the to raise
patient
the patient for intubation. It is noteworthy that during this period of high
for intubation. It is noteworthy that during this period of high physical activity, the NSH continued physical activity, the NSto
H

continued to rise, suggesting that EMG was not the constitutional contributor
rise, suggesting that EMG was not the constitutional contributor to the decreased NSH in this episode. to the decreased NS H

in this episode.
Entropy 2016, 18, 427 10 of 15
Entropy 2016, 18, 427 10 of 15

Figure7.7. Session
Figure Sessiondetails
detailsfor
forneurodynamic
neurodynamic entropy
entropydecreases.
decreases.ThreeThree
simulation episodes
simulation are shown
episodes are
aroundaround
shown periods of decreasing
periods NSH. The
of decreasing NSH .first
Thesegment (A) lasted
first segment 100 s and
(A) lasted 100 sbegan at 215ats 215
and began of the
s
ofperformance;
the performance;the second segment
the second (B) lasted
segment (B) 140 s and
lasted 140began
s and at 340 satof340
began the sperformance; and, the
of the performance;
third
and, thesegment (C) lasted
third segment 120 s and
(C) lasted 120 sbegan at 540at s540
and began of sthe performance.
of the performance.TheThecaptions describe
captions the
describe
problem
the problem thethe
team was
team addressing
was addressing in in
each segment.
each segment.

Thethird
The thirdepisode
episodeofofdecreased
decreasedNS NSHbegan
beganwith
withthetheintubation
intubationof ofthe
thepatient
patientby
byTeam
TeamMember
Member11
H
(540660 s) (Figure 7C). For this figure, the NS H decreases are shown for 16 Hz, as from Figure 5 this
(540660 s) (Figure 7C). For this figure, the NSH decreases are shown for 16 Hz, as from Figure 5
waswas
this the the
period of the
period lowest
of the NSHNS
lowest at 16atHz.
16 During intubation,
Hz. During the NS
intubation, theH rose and the 16 Hz EEG power
NSH rose and the 16 Hz EEG
H
power levels of Team Member 1 remained around average values; i.e., theintubation
levels of Team Member 1 remained around average values; i.e., the intubation process wasnot
process was not
associatedwith
associated withlow
lowNSNSH. .The
Thepatients
patientsbreathing
breathingremained
remainedwheezy
wheezyuntil
untilthe
theteam
teamrealized
realizedthe
theoxygen
oxygen
H
tube was unplugged. After re-attaching the line, the NS H began to rise as the team discussed how to
tube was unplugged. After re-attaching the line, the NSH began to rise as the team discussed how to
controlthe
control thecontinuing
continuingseizures.
seizures.

3.4.Neurodynamic
3.4. NeurodynamicOrganizations
Organizations
Theprior
The priorstudies
studies demonstrated
demonstrated important
important properties
properties of team
of team neurodynamics
neurodynamics in that
in that decreased
decreased NS
NS entropy
entropy equalsequals less uncertainty
less uncertainty about the about thethe
state of state
teamofand
theequals
team more
and equals more neurodynamic
neurodynamic organization.
organization.
To better convey Tothese
better convey these
relationships, relationships,
the periods the periods
of increased of increased
neurodynamic neurodynamic
organization can be
organization
expressed can beterms
in positive expressed in positive
by subtracting theterms by subtracting
NS entropy the NS obtained
from the entropy entropy when
from the entropy
the symbol
obtained
streams when
were the symbol
randomized streams
prior were randomized
to calculating the entropy prior to calculating
levels. the entropy
These quantitative levels.ofThese
estimates the
quantitative estimates of the teams neurodynamic organization (ND
teams neurodynamic organization (ND ) reflect periods of increased order where fewer ) reflect periods of increased
symbols
order
are where
being fewer symbols
expressed. The NDare forbeing expressed. teams
four healthcare The ND for fourinhealthcare
are shown Figure 8, withteams are shown in
a performance
Figure 8, with a performance highlighted in this paper in Figure
highlighted in this paper in Figure 8A. Across the different performances, the ND was 8A. Across thegenerally
different
performances, the ND was generally higher in the Briefing and Debriefing
higher in the Briefing and Debriefing segments than in the Scenarios, a finding similar to what
segments than inwe
the
Scenarios,
observed inasubmarine
finding similar to what
navigation we observed
teams [15]. in submarine navigation teams [15].
Entropy 2016, 18, 427 11 of 15
Entropy 2016, 18, 427 11 of 15

Figure 8. Neurodynamic
Figure 8. Neurodynamic organization
organization profiles. The NS
profiles. The NSH from the performances by (A) team J10T2;
H from the performances by (A) team J10T2;
(B)
(B) team J10T3; (C) team J5S1; and, (D) team J4S1were averaged across
team J10T3; (C) team J5S1; and, (D) team J4S1were averaged across all
all sensors
sensors and
and frequencies
frequencies
and
and subtracted from the average of similar profiles from NS that were randomized before the
subtracted from the average of similar profiles from NS that were randomized before the entropy
entropy
was
was determined.
determined.

4.
4. Discussion
Discussion
The
The emerging
emerging picture
picture ofof teams
teams fromfrom these
these and
and previous
previous studies
studies isis one
one of
of evolving
evolving dynamics
dynamics thatthat
are
are continually punctuated by small and large fluctuations as teams encounter disturbances
continually punctuated by small and large fluctuations as teams encounter and resolve and resolve
to their normal
disturbances rhythms.
to their normalNeurodynamic
rhythms. Neurodynamicorganizational models capture
organizational these
models changing
capture thesedynamics
changing
across levels and time scales of teamwork and relate them to observable
dynamics across levels and time scales of teamwork and relate them to observable performance performance behaviors
indicative
behaviors of team performance
indicative in ways thatinappear
of team performance applicable
ways that appeartoapplicable
a variety of to teamwork situations.
a variety of teamwork
In this study, we have shown that healthcare teams performing simulations based on patient
situations.
ventilation
In thisshow
study,neurodynamic
we have shown entropy fluctuations
that healthcare of similar
teams magnitudes
performing and durations
simulations based onaspatient
those
observed
ventilationpreviously with submarine
show neurodynamic entropy navigation teams.
fluctuations The origin
of similar of these fluctuations
magnitudes and durations centers on
as those
the establishment and persistence of temporal organizations where the frequency-specific
observed previously with submarine navigation teams. The origin of these fluctuations centers on EEG power
relationships between
the establishment and team members
persistence transiently
of temporal stabilize. These
organizations relationships
where are not synchronized
the frequency-specific EEG power in
the sense of frequency
relationships betweenor phase
team locking transiently
members where each stabilize.
team member Theseshares the sameare
relationships frequency, phase and
not synchronized
topology of a particular EEG rhythm, i.e., the rhythmic patterns do not necessarily
in the sense of frequency or phase locking where each team member shares the same frequency, phase need to coincide or
overlap exactly.of a particular EEG rhythm, i.e., the rhythmic patterns do not necessarily need to
and topology
A framework
coincide for understanding the meso- and micro-scale temporal dynamics of teams
or overlap exactly.
emerges from the neurodynamically
A framework for understanding the linked ideas
meso- andofmicro-scale
brain wavetemporal
synchronization/entrainment
dynamics of teams emerges [32],
and
fromacross-brain social couplings
the neurodynamically linked [33].
ideasOne ofpossibility
brain wave is synchronization/entrainment
that the rhythm of the team had been
[32], andcaptured
across-
or
brain social couplings [33]. One possibility is that the rhythm of the team had been capturedhas
entrained by the task situation/events and/or the actions of other members. Entrainment or
been defined
entrained by bythe[34]
task(p. 149), as the .and/or
situation/events . . process in which
the actions ofthe rhythms
other members.displayed by twohas
Entrainment or more
been
phenomena
defined by [34]become synchronized,
(p. 149), as the processwith one of thethe
in which rhythms
rhythms often being more
displayed by two powerful
or moreor dominant
phenomena
and capturing the rhythm of the other.
become synchronized, with one of the rhythms often being more powerful or dominant and
capturing the rhythm of the other.
It is well established that some electrical rhythms of the brain synchronize to external repetitive
sounds/images [35,36]. These synchronizations can be a simple reflection of the periodicity of the
Entropy 2016, 18, 427 12 of 15

It is well established that some electrical rhythms of the brain synchronize to external repetitive
sounds/images [35,36]. These synchronizations can be a simple reflection of the periodicity of the
stimulus sequence, more complex rates of coordinated percepto-motor behaviors like the production
of, or listening to music, finger tapping, or sentence comprehension [37,38], or may include very
complex within and across-brain rhythms as teams synchronize with the task and other team members.
Hasson et al. [39] extended these ideas to more complex situations by having individuals view scenes
from a movie. As the video unfolded, the embedded visual and auditory elements entrained the
subjects cognition with inter-subject synchronizations occurring in the visual, auditory and cortical
brain regions. Such synchronization has been repeatedly seen with subjects viewing movie clips [40],
especially when those clips contained emotionally rich scenes [41].
Our studies point to teams undergoing neurodynamic organizations during similar emotionally
laden-situations, i.e., when there was the need for the team to resolve uncertainty or make a decision.
This was primarily seen with gamma oscillations, which have been proposed to be important
mechanisms for active maintenance of working memory information [20].
An increase in alpha rhythm power, termed event-related synchronization (ERS), reflects cortical
inhibition in the brain regions that are task-irrelevant or potentially interfering processes, i.e., brain
regions not directly involved in responding to a stimulus. The decrease in alpha amplitude/power
reflects release from inhibition with the magnitude of ERD reflecting the degree of cortical
activation [18]. Alpha and gamma frequency oscillations also occur in the same brain regions and
interact with each other through cross-frequency coupling in a complex relationship, such that when
there is extensive cortical activation (high alpha band levels), gamma rhythm-driven working memory
is suppressed [20]. The negative correlation between alpha power and gamma power shown in
Figure 3B likely reflects this cross-frequency coupling.
The detailed dynamics of the team shown in Figure 7, where neurodynamic organization
increases during periods of uncertainty and decreases once the uncertainty is resolved, are consistent
with previous studies with submarine navigation teams indicating that the largest neurodynamic
organizations occurred during stressful periods [15,16,25].
These studies expand the potential usefulness of neurodynamic symbols as intermediate
representations of team function, by showing that similar principles are operational across multiple
teams performing in multiple domains. In this regard, it is worth noting that while the overall principles
of team neurodynamics are similar across high school problem-solving, submarine navigation and
healthcare teams, differences are seen in the relative proportion of ND in the alpha, beta and gamma
frequency bands. The map navigation task performed by high school students is rich in mental
imagery, as one student uses speech and gestures to help a second student navigate a path through
landmarks on a map. This task primarily results in beta and gamma neurodynamic organizations [22].
The activity level and crew size of submarine navigation teams requires rapid transfer and integration
of information across a team whose members hold different pieces of information; these dynamics
primarily resulted in alpha and gamma neurodynamic organizations. Finally, the healthcare teams
work more from a shared knowledge base and are involved in dynamic problem solving; here,
the ND in the gamma band predominates. While there are exceptions to these generalizations,
overall, they suggest that the nature of the task recruits specific forms of neurodynamic coordination,
perhaps providing an avenue for more precise training activities designed to enhance specific
ND skills.

5. Conclusions
The similarities in the neurodynamics of healthcare and submarine navigation teams suggests
that team neurodynamics may be a fundamental component of teamwork, providing a quantitative
framework that may enable comparisons to be made across different kinds of teams, tasks,
missions, platforms and environments. These studies may have particular relevance for healthcare
teams, where professionals are continually plagued by uncertainty when attending to patients [42].
Entropy 2016, 18, 427 13 of 15

In particular, a teams neurodynamics may provide an opportunity to monitor uncertainty in healthcare

teams in near real-time.

Acknowledgments: The authors thank the participating staff and students of the Order of Saint Francis Hospital
community for their logistical and technical support for these studies. The studies were supported in part by
the JUMP Foundation for Simulation Research and the Defense Advanced Research Projects Agency under
contract W31P4QC0166.
Author Contributions: All authors helped conceive, design and perform the experiments; R.S. and T.G. analyzed
the data and wrote the paper. A.W.-D and D.H. reviewed the manuscript and provided the logistical support and
space for the experiments. All authors have read and approved the final manuscript.
Conflicts of Interest: The authors declare no conflict of interest. The funding sponsors had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the
decision to publish the results.

Glossary of Terms

symbolic representations of the momentary EEG power levels of

Neurodynamic Symbols (NS)
Neurodynamic Symbol States (NSS)
Neurodynamic Data Streams (NDS)
Neurodynamic Entropy (NSH )
Neurodynamic Organization (ND )
a neurodynamic marker for each team member
a collection of NS that together describe a team performance
the second-by-second concatenated sequences of NS that
temporally span a task performed by the team
a quantitative measure of the distributions of NS in a NDS when
examined over a moving window of time, often 60100 s
a quantitative estimate of organization reflecting periods of
increased neurodynamic order. ND is calculated by subtracting
the Shannon entropy of the NDS obtained over a 60 s or 100 s
moving window from the entropy of the NS stream after it has
been randomized (i.e., ND = NSH random NSH )

References
1. Cooke, N.J.; Gorman, J.C.; Kiekel, P. Communication as team-level cognitive processing. In Macrocognition in
Teams; Letsky, M.P., Warner, N.W., Fiore, S.M., Smith, C.A.P., Eds.; Ashgate Publishing Ltd.: Burlington, VT,
USA, 2008.
2. Schippers, M.; Roebroeck, A.; Renken, R.; Nanetti, L.; Keysers, C. Mapping the information flows from
one brain to another during gestural communication. Proc. Natl. Acad. Sci. USA 2010, 107, 93889393.
[CrossRef] [PubMed]
3. Caetano, G.; Jousmaki, V.; Hari, R. Actors and observers primary motor cortices stabilize similarly after
seen or heard motor actions. Proc. Natl. Acad. Sci. USA 2007, 104, 90589062. [CrossRef] [PubMed]
4. Shockley, K.; Santana, M.-V.; Fowler, C.A. Mutual interpersonal postural constraints are involved in
cooperative conversation. J. Exp. Psychol. Hum. Percept. Perform. 2003, 29, 326332. [CrossRef] [PubMed]
5. Anders, S.; Heinzle, J.; Weiskopf, N.; Ethofer, T.; Haynes, J. Flow of affective information between
communicating brains. Neuroimage 2011, 54, 439446. [CrossRef] [PubMed]
6. Menoret, M.; Varnet, L.; Fargier, R.; Cheylus, A.; Curie, A.; des Portes, V.; Nazir, T.A.; Paulignan, U.
Neural correlates of non-verbal social interactions: A dual-EEG study. Neurophyschologia 2014, 55, 8591.
[CrossRef] [PubMed]
7. Gardezi, F.; Lingard, L.; Espin, S.L.; Whyte, S.; Orser, B.; Baker, G.R. Silence, power and communication in
the operating room. J. Adv. Nurs. 2009, 65, 13901399. [CrossRef]
8. Tognoli, E.; Kelso, J.A. The coordination dynamics of social neuromarkers. arXiv, 2015, arXiv:1310.7275.
9. Palva, J.M.; Zhigalov, A.; Hirvonen, J.; Korhonen, O.; Linkenkaer-Hansen, K.; Palva, S. Neuronal long-range
temporal correlations and avalanche dynamics are correlated with behavioral scaling laws. Proc. Natl. Acad.
Sci. USA 2013, 110, 35653590. [CrossRef] [PubMed]
10. Proekt, A.; Banavar, J.R.; Maritan, A.; Pfaff, D.W. Scale invariance in the dynamics of spontaneous behavior.
Proc. Natl. Acad. Sci. USA 2012, 109, 1056410569. [CrossRef] [PubMed]
11. Gilden, D.L.; Thornton, T.; Mallon, M.W. 1/f noise in human scaling. Science 1995, 5205, 18371839. [CrossRef]
Entropy 2016, 18, 427 14 of 15

12. Van Orden, G.C.; Holden, J.G.; Turvey, M.T. Human cognition and 1/f scaling. J. Exp. Psychol. 2005, 134,
117133. [CrossRef] [PubMed]
13. Butner, J.; Pasupathi, M.; Vallejos, V. When the facts just dont add up: The fractal nature of conversational
stories. Soc. Cogn. 2008, 26, 670699. [CrossRef]
14. Flack, J.C. Multiple time-scales and the developmental dynamics of social systems. Philos. Trans. R. Soc. B
Biol. Sci. 2012, 367, 18021810. [CrossRef] [PubMed]
15. Stevens, R.H.; Galloway, T.; Wang, P.; Berka, C.; Tan, V.; Wohlgemuth, T.; Lamb, J.; Buckles, R. Modeling the
neurodynamic complexity of submarine navigation teams. Comput. Math. Organ. Theory 2012, 19, 346369.
[CrossRef]
16. Stevens, R.H.; Galloway, T. Modeling the neurodynamic organizations and interactions of teams.
Soc. Neurosci. 2015, 11, 123139. [CrossRef] [PubMed]
17. Hari, R. Action perception connection and the cortical mu-rhythm. Prog. Brain Res. 2006, 159, 253260.
[PubMed]
18. Klimesch, W.; Sauseng, P.; Hanslmayr, S. EEG alpha oscillations: The inhibition-timing hypothesis.
Brain Res. Rev. 2007, 53, 6388. [CrossRef] [PubMed]
19. Klimesch, W. Alpha-band oscillations, attention and controlled access to stored information. Trends Cogn. Sci.
2012, 16, 606617. [CrossRef] [PubMed]
20. Roux, F.; Uhlhaas, P. Working memory and neural oscillations: Alpha-gamma versus theta-gamma codes for
distinct WM information? Trends Cogn. Sci. 2014, 18, 1625. [CrossRef] [PubMed]
21. Bonnefond, M.; Jensen, O. Gamma activity coupled to alpha phase as a mechanism for top-down controlled
gating. PLoS ONE 2015, 10, e012866. [CrossRef] [PubMed]
22. Stevens, R.H.; Galloway, T. Toward a quantitative description of the neurodynamic organizations of teams.
Soc. Neurosci. 2014, 9, 160173. [CrossRef] [PubMed]
23. Fishel, S.R.; Muth, E.R.; Hoover, A.W. Establishing appropriate physiological baseline procedures for
real-time physiological measurement. J. Cogn. Eng. Decis. Mak. 2007, 1, 286308. [CrossRef]
24. Shannon, C.E. Prediction and entropy of printed English. Bell Syst. Tech. J. 1951, 30, 5064. [CrossRef]
25. Stevens, R.H.; Gorman, J.C.; Amazeen, P.; Likens, A.; Galloway, T. The organizational dynamics of teams.
Nonlinear Dyn. Psychol. Life Sci. 2013, 17, 6786.
26. Likens, A.D.; Amazeen, P.G.; Stevens, R.; Galloway, T.; Gorman, J.C. Neural signatures of team coordination
are revealed by multifractal analysis. Soc. Neurosci. 2014, 9, 219234. [CrossRef] [PubMed]
27. Delorme, A.; Palmer, J.; Onton, J.; Oostenveld, R.; Makeig, S. Independent EEG sources are dipolar. PLoS ONE
2012, 12, e30135. [CrossRef] [PubMed]
28. Yong, X.; Ward, R.K.; Birch, G.E. Facial EMG contamination of EEG signals: Characteristics and effects of
spatial filtering. In Proceedings of the IEEE 3rd International Symposium on Communications, Control and
Signal Processing (ISCCSP), St. Julians, Malta, 1214 March 2008.
29. Baker, D.P.; Amodeo, A.M.; Krokos, K.J.; Slonim, A.; Herrera, H. Assessing teamwork attitudes in healthcare:
Development of the TeamSTEPPS teamwork attitudes questionnaire. Qual. Saf. Health Care 2010, 19, e49.
[CrossRef] [PubMed]
30. Oostenveld, R.; Fries, P.; Maris, E.; Schoffelen, J.-M. FieldTrip: Open source software for advanced analysis
of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 2011, 156869. [CrossRef]
[PubMed]
31. Delorme, A.; Sejnowski, T.; Makeig, S. Enhanced detection of artifacts in EEG data using higher-order
statistics and independent component analysis. Neuroimage 2007, 34, 14431449. [CrossRef] [PubMed]
32. Will, U.; Berg, E. Brainwave synchronization and entrainment to periodic stimuli. Neurosci. Lett. 2007, 424,
5560. [CrossRef] [PubMed]
33. Hasson, U.; Ghazanfar, A.; Glantucci, B.; Garrod, S.; Keysers, C. Brain-to-brain coupling: A mechanism for
creating and sharing a social world. Trends Cogn. Sci. 2011, 17, 413425. [CrossRef] [PubMed]
34. Bluedorn, A.C. The Human Organization of Time: Temporal Realities and Experience; Stanford University Press:
Stanford, CA, USA, 2002.
35. Adrian, E.D.; Matthews, B.H.C. The interpretation of potential waves in the cortex. J. Physiol. 1934, 81,
440471. [CrossRef] [PubMed]
36. Galambos, R.; Makeig, S.; Talmachoff, P.J. A 40-Hz auditory potential recorded from the human scalp.
Proc. Natl. Acad. Sci. USA 1981, 78, 26432647. [CrossRef] [PubMed]
Entropy 2016, 18, 427 15 of 15

37. Van Noorden, L.; Moelants, D. Resonance in the perception of musical pulse. J. New Music Res. 1999, 28,
4366. [CrossRef]
38. Moreno, I.; de Vega, M.; Len, I. Understanding action language modulates oscillatory mu and beta rhythms
in the same way as observing actions. Brain Cogn. 2013, 82, 236242. [CrossRef] [PubMed]
39. Hasson, U.; Nir, Y.; Levy, I.; Fuhrmann, G.; Malach, R. Inter-subject synchronization of cortical activity
during natural vision. Science 2004, 303, 16341640. [CrossRef] [PubMed]
40. Nummenmaa, L.; Gleran, E.; Viinikainen, M.; Jaaskelainen, P.; Hari, R.; Sams, M. Emotions promote social
interaction by synchronizing brain activity across individuals. Proc. Natl. Acad. Sci. USA 2012, 109, 95999604.
[CrossRef] [PubMed]
41. Dmochowski, J.P.; Sajda, P.; Dias, J.; Parra, L. Correlated components of ongoing EEG point to emotionally
laden attentionA possible marker of engagement? Front. Hum. Neurosci. 2012, 6, 112. [CrossRef] [PubMed]
42. Wray, C.M.; Loo, L.K. The diagnosis, prognosis and treatment of medical uncertainty. J. Med. Educ. 2015, 7,
523527. [CrossRef] [PubMed]

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