Facilitating Neurofeedback in Children with Autism and Intellectual Impairments Using TAGteach

Abstract

Individuals with autism and intellectual impairments tend to be excluded from research due to their difficulties with methodological compliance. This study focuses on using Teaching with Acoustic Guidance-TAGteach-to behaviorally prepare children with autism and a IQ ≤ 80 to participate in a study on neurofeedback training (NFT). Seven children (ages 6-8) learned the prerequisite skills identified in a task analysis in an average of 5 h of TAGteach training, indicating that this is a feasible method of preparing intellectually-impaired children with autism to participate in NFT and task-dependent electroencephalography measures. TAGteach may thus have the potential to augment this population's ability to participate in less accessible treatments and behavioral neuroscientific studies.

Full text

1 23
Journal of Autism and
Developmental Disorders
ISSN 0162-3257
Volume 48
Number 6
J Autism Dev Disord (2018)
48:2090-2100
DOI 10.1007/s10803-018-3466-4
Facilitating Neurofeedback in Children
with Autism and Intellectual Impairments
Using TAGteach
Kristen LaMarca, Richard Gevirtz, Alan
J.Lincoln & Jaime A.Pineda

1 23
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Vol:.(1234567890)
Journal of Autism and Developmental Disorders (2018) 48:2090–2100
https://doi.org/10.1007/s10803-018-3466-4
1 3
ORIGINAL PAPER
Facilitating Neurofeedback inChildren withAutism andIntellectual
Impairments Using TAGteach
KristenLaMarca1,3· RichardGevirtz1· AlanJ.Lincoln1· JaimeA.Pineda2
Published online: 27 January 2018
© Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
Individuals with autism and intellectual impairments tend to be excluded from research due to their difficulties with meth-
odological compliance. This study focuses on using Teaching with Acoustic Guidance—TAGteach—to behaviorally prepare
children with autism and a IQ ≤ 80 to participate in a study on neurofeedback training (NFT). Seven children (ages 6–8)
learned the prerequisite skills identified in a task analysis in an average of 5h of TAGteach training, indicating that this is
a feasible method of preparing intellectually-impaired children with autism to participate in NFT and task-dependent elec-
troencephalography measures. TAGteach may thus have the potential to augment this population’s ability to participate in
less accessible treatments and behavioral neuroscientific studies.
Keywords Autism· Low-functioning· Intellectual impairment· TAGteach· Conditioned reinforcement· Auditory
secondary reinforcement· Mirror neurons· Mu rhythms· Neurofeedback
Introduction
Autism Spectrum Disorder (ASD)—a neurodevelopmental
condition characterized by social-communication deficits,
and restrictive or repetitive behaviors (American Psychi-
atric Association 2013)—is currently estimated to affect
15 per 1000 children (Christensen etal. 2016). The highly
heterogeneous nature of impairments and range of sever-
ity, along with an elevated rate of comorbidities (Hofvander
etal. 2009; Lugnegard etal. 2011; Simonoff etal. 2008),
complicate the understanding, treatment, and study of the
disorder. While the standard behavioral interventions for
autism show improvements in psychosocial outcomes, they
tend to be costly, time-consuming, and limited in efficacy
(Krebs-Seida 2009). Prognosis is generally poor in terms
of social, occupational, and independent functioning later
in life. This is particularly true for those who have more
intellectual or language deficits (Ben-Itzchak and Zachor
2011; Howlin etal. 2013; Levy and Perry 2011; Matson and
Shoemaker 2009).
Numerous neurobiological anomalies in ASD have been
identified (Anagnostou and Taylor 2011; Parellada etal.
2013) though the cause remains unknown. The disorder is
thought to arise from a wide variety of genetic and environ-
mental factors that play a role in the diverse expression of
phenotypic traits (Hall and Kelley 2013). Converging find-
ings from brain imaging research have given rise to theories
on the neuroetiology of ASD. Studies on functional commu-
nication across brain networks have been reporting patterns
of hypo-coherence in long-range default mode networks,
inter- and intra- hemispheric hypo-connectivity, and hyper-
connectivity in local and long-distance networks (Kahn etal.
2015; Mohammad-Rezazadeh etal. 2016; Müller etal. 2011;
Rane etal. 2015), although the methodologies applied and
results reported have been inconsistent. Moreover, the man-
ner in which dysfunctional connectivity specifically impacts
core ASD symptoms or the degree of severity has not been
clearly delineated thus far.
This manuscript is based on the doctoral dissertation of the first
author. Preliminary data from this study was included in the
publication, Pineda etal. (2014b).
* Kristen LaMarca
kristenlamarca@outlook.com
1 Department ofClinical Psychology, California School
ofProfessional Psychology, Alliant University, SanDiego,
CA, USA
2 Department ofCognitive Neuroscience, University
ofCalifornia, SanDiego, CA, USA
3 Vista, CA92081, USA
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2091Journal of Autism and Developmental Disorders (2018) 48:2090–2100
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An alternate framework has linked ASD social impair-
ments with abnormal activation during action observation
of the mirror neuron system (MNS) and 8–12Hz electroen-
cephalographic (EEG) frequency band (mu) over the sen-
sorimotor cortex, which is proposed to index MNS activity
(see Pineda etal. 2012, 2014b). While research on the MNS
and mu suppression has garnered support generally and as
related to ASD deficits (Arnstein etal. 2011; Bernier etal.
2007; Dapretto etal. 2006; di Pellegrino etal. 1992; Fox
etal. 2016; Iacoboni and Dapretto 2006; Mukamel etal.
2010; Perkins etal. 2010; Oberman etal. 2005, 2013; Pineda
2005a, b; Williams etal. 2001), it has also been a prominent
subject of scientific debate with a number of researchers
providing contradictory evidence and alternative viewpoints
(Enticott etal. 2013; Dinstein etal. 2010; Hamilton 2013;
Hickock 2009; Hobson and Bishop 2016; Mostofsky etal.
2006; Stiegliz Ham etal. 2011).
Limitations to traditional behavioral therapies and emerg-
ing neuroetiological theories have led researchers to explore
if neurofeedback training (NFT) can normalize the electro-
physiological profiles of individuals with ASD, thereby
reducing core symptomology. NFT uses a brain-computer
interface system to display real-time electrophysiological
signals to users—usually in the form of a game—to facilitate
the self-regulation of EEG through operant learning (Marz-
bani etal. 2016). The applications of NFT are widespread,
and efficacy evidence is available for a variety of disorders
associated with abnormal electrophysiology (LaVaque and
Moss 2003), such as epilepsy (Tan etal. 2009; Walker 2008)
and attention deficit-hyperactivity disorder (Cortese etal.
2016; Mayer and Arns 2016).
Several NFT studies of individuals with ASD have shown
positive changes in social behavior, attention, and connec-
tivity using various protocols guided by clinical symptoms
or individualized based on a quantitative EEG assessment
(For a review, see Coben etal. 2010, 2014; or; Pineda etal.
2012). NFT research from our laboratory, reviewed in more
detail by Pineda etal. (2014a), has targeted mu waves by
up-training 8–12Hz rhythms over the central motor strip
while inhibiting beta and theta waves (which are associ-
ated with general movement and eye blinks, respectively).
Results suggest that learning to control mu-related oscil-
lations though NFT can normalize mu suppression during
action observation tasks and improve behavior in individuals
with ASD and an IQ > 80 (Datko etal. 2017; Pineda etal.
2008; Pineda etal. 2014a; Friedrich etal. 2015). Relevant
criticisms of these studies have highlighted potential con-
founds, such as the control of attentional factors, highly
localized evidence of the effect NFT on neurophysiology,
and the overlap of occipital alpha with the mu frequency
band. Additional, contrasting views on connectivity and mu-
based NFT paradigms in ASD are discussed by Holtmann
etal. (2011). Although there is a need for clearer theoretical
and empirical alignment between the electrophysiological
targets of NFT and core symptoms, NFT for ASD overall
(whether the protocol targets mu activity or other local or
more broadly distributed functional networks) appears to be
a promising, noninvasive means of clinically intervening at
the neurobiological level as opposed to solely focusing on
the behavioral manifestations of the disorder.
Nevertheless, many individuals with ASD may not have
the prerequisite behavioral, language or cognitive skills nec-
essary to participate in therapies that might improve their
symptoms or condition. While those with a higher degree
of severity have the greatest need for effective treatments,
these individuals tend to be understudied due to their dif-
ficulties with methodological compliance and ability to
provide useful data. Thus, the literature on ASD overall,
and as related to NFT, is more inclusive of high functioning
individuals rather than those described as low functioning,
often defined by investigators as an IQ below 70 or 80. There
is a strong need to develop novel, empirically-based methods
for behaviorally preparing intellectually-impaired individu-
als with ASD to participate in more experimental research
and improve their ability to engage in less accessible clinical
interventions, such as NFT.
Teaching with Acoustic Guidance (TAGteach) is a novel
teaching tool that is simple to learn and implement, and
appears to have the potential to facilitate lower-function-
ing children’s participation in more treatment and research
studies. The method is based on the classical and operant
principles that have been central to autism treatment for
decades (Granpeesheh etal. 2009; Skinner 1953), and uses
conditioned auditory markers to shape complex behavioral
sequences in successive approximations (http://www.TAGte
ach.com). The auditory marker is optimal for a population
with the social-communication impairments inherent in
autism because it removes the social and language features
of verbal praise. The sound marker is also more distinct and
temporally precise in reinforcing target behaviors than verbal
communication (Vargas 2009).
TAGteach interventions are structured to be flexible,
individualized, and arranged for high success rates (Vargas
2009). Caregiver involvement is encouraged in the concep-
tual teaching of a tag point, which is defined as the single,
observable action currently being trained. Trainers gener-
ally abide by the three-try rule, meaning that if the learner
fails to perform an action three times, then the trainer can
return to a point of success by choosing a more achievable
tag point. Tag points are described in five words or less and
attempts are made to devise tag points that resolve more
than one problematic behavior, known as value-added tag
points; for instance, the tag point of “put hands in pockets”
could potentially resolve a multitude of behaviors, such as
nail biting or hand flapping. TAGteach invites participants to
be involved in the naming of tag points, and also emphasizes
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the offering of behavioral choices to learners to improve
their participation in performing tasks. Training sessions
should be shorter in duration to avoid focus fatigue, which
occurs when the learner’s ability to focus on task-learning
deteriorates because the duration of a training session is too
long.
Through an AB design, Barbera (2010) showed it was
possible to teach a 14year-old with moderate to severe
autism who had been unable to learn to tie his shoes to
do so after 90min of TAGteach. Morien and Eshelman
(2010) examined sign-language behaviors and the number
of prompts required during signing trials in three nonverbal
children with autism (ages 6–9) across three communication
training conditions that included access to primary reinforc-
ers and verbal praise (1) at fixed intervals (Non-Contingent
Reinforcement; NCR), (2) immediately following a correct
response (Contingent Reinforcement; CR), and (3) after
auditory marking of a target behavior (TAGteach). With
ratings of treatment integrity and interobserver agreement
all above 97%, their results showed that TAGteach was more
effective at eliciting sign-language than the CR or NCR con-
ditions, and required prompting as much as the CR condition
did and at a lower rate than the NCR condition. For a review
of other case reports that support TAGteach in autism popu-
lations, see Pineda etal. (2014a).
In the present study, we sought to evaluate the feasibility
of using TAGteach to quickly prepare children with ASD
and an IQ ≤ 80 to perform skills required to participate in
a neurofeedback intervention (as discussed in Pineda etal.
2008, 2014a) and the corresponding behavioral tasks of an
encephalographic (EEG) imaging test, the mu suppression
index1 (MSI; see Oberman etal. 2005).
Methods
Design andParticipants
We employed a case-series design that used TAGteach to
train participants to perform prerequisite skills of NFT and
the MSI in 6h or less. Participants were seven boys and
one girl, ages 6–8 (M = 6.9 ± .8years) that met DSM-IV-TR
criteria for Autistic Disorder (American Psychiatric Asso-
ciation 2013). Diagnoses were based on the judgement of
an expert clinician and met cut-off criteria for autism using
standard diagnostic tests—the Autism Diagnostic Interview
Revised (ADI-R; Lord etal. 1994) and Autism Diagnostic
Observation Schedule (ADOS; Lord etal. 2002). Full scale
IQ scores, according to the Wechsler Abbreviated Scale of
Intelligence (WASI; Wechsler 1999), ranged from 58 to 80
(M = 69 ± 8) while verbal IQ and performance IQ ranged
from 58 to 76 (M = 66 ± 6) and 63 to 99 (M = 78 ± 14),
respectively. One participant was dropped from the study
after beginning TAGteach due to a medical problem. Table1
provides descriptive data on individual cases.
Participants were recruited through a private San Diego
agency and a local autism e-newsletter. Each individual was
required to show an inability or unwillingness to perform all
prerequisite behaviors volitionally or with incentives. The
Institutional Review Board of Alliant International Univer-
sity, San Diego approved the study.
Procedures
TAGteach‑Assisted Behavioral Preparation
We used TAGteach to train four core skills (see below) that
were required to participate in a subsequent study on mu
rhythm neurofeedback training (NFT). These prerequisite
skills were broken down into 26 discrete behaviors in a
task analysis. The prerequisite skills had to be sustained for
120s for the participant to meet behavioral criteria, and were
defined as follows:
1. Participant sits still and quietly in a chair.
2. Participant tolerates electrodes and skin preparation pro-
cedures.
3. Participant performs a motor task of slowly opening and
closing the right hand.
4. Participant visually attends to a display screen with
video stimuli.
During the baseline assessment of participants’ ability
to perform prerequisite skills, we used verbal praise to pro-
mote compliance, and if unsuccessful, parents offered pri-
mary reinforcers (e.g., food and access to toys) as incentives.
Participants were offered up to three trials to demonstrate a
requested behavior.
We next introduced TAGteach, and structured sessions to
last an hour or less. After each session, participants received
a score of 1 or 0 for each of the 26-items of the task analysis
to indicate if they did or did not demonstrate a behavioral
criterion. We trained attention to visual stimuli using a video
of a circle shape oscillating from left to right. When par-
ticipants met all task analysis criteria at least one time, they
underwent NFT and MSI testing as part of another study
(LaMarca etal. 2013).
1 The Mu Suppression Index (MSI; Oberman et al. 2005) assesses
changes in EEG mu power in response to observing four 120 s vid-
eos of different types of movement: non-biological, biological,
goal-direction, and social. A ratio of power is calculated for the
four motion observation conditions relevant to a resting baseline,
and an action execution condition. Ratio data are transformed with
a log algorithm, such that positive and negative values indicated mu
enhancement and suppression, respectively.
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TAGteach‑Assisted Mu Suppression Testing
During MSI testing, participants earned tag points by
observing or executing specific motions, and by com-
pleting a resting baseline. Each participant had a single
attempt to maintain his/her visual attention when action
observation stimuli were presented, though the resting
baseline and the action execution tasks were conducted
more than once if needed since these tasks were not
impacted by habituation to stimuli. We used TAGteach to
facilitate MSI testing three times (pre-test, post-test, and
follow-up) to assess mu rhythm changes from NFT in the
subsequent study.
TAGteach‑Assisted Neurofeedback
To participate in the NFT intervention, participants were
to complete a total of 30min of NFT twice per week for
approximately 20weeks. Participants earned tag points for
completing a resting baseline at the start of each NFT ses-
sion, and for completing an NFT segment, each of which
ranged from 2.5 to 10min. Participants were rewarded for
Table 1 Descriptive
characteristics of individual
cases
WASI Wechsler abbreviated scale of intelligence, FS full scale, V verbal, P performance, ADI-R autism
diagnostic interview—revised, ADOS autism diagnostic observation schedule, S social, C communication,
NV nonverbal, R restricted, repetitive, stereotyped behavior or interests, I imagination/creativity, P play
Case Age, sex WASI IQ [95% CI] ADI-R algorithm ADOS
module/
algorithm
RC 7years, male FS: 73 [68, 80]
V: 72 [67, 82]
P: 79 [73, 87]
S: 24
C: 21 (V)
R: 11 (NV)
Onset: 3
Module 3
C: 5
S: 14
I: 2
R: 6
CR 6years, male FS: 80 [75, 86]
V: 68 [63, 77]
P: 99 [92, 106]
S: 30
C: 19 (V)
11 (NV)
R: 11
Onset: 4
Module 2
C: 7
S: 11
I: 0
R: 2
ZB 7years, male FS: 73 [68, 80]
V: 76 [70, 85]
P: 74 [69, 82]
S: 21
C: 20 (V)
11 (NV)
R: 11
Onset: 2
Module 3
C: 8
S: 14
I: 2
R: 7
SR 7years, female FS: 63 [59, 70]
V: 61 [56, 71]
P: 70 [65, 79]
S: 26
C: 20 (V)
13 (NV)
Onset: 4
Module 1
C: 7
S: 10
P: 1
R: 4
XD 8years, male FS: 58 [54, 65]
V: 58 [54, 68]
P: 64 [59–73]
S: 29
C: 20 (V)
11 (NV)
R: 10
Onset: 5
Module 1
C: 5
S: 9
I: 0
R: 4
SK 6years, male FS: 72 [67, 79]
V: 67 [62, 67]
P: 83 [77, 91]
S: 27
C: 22 (V)
14 (NV)
R: 13
Onset: 3
Module 1
C: 4
S: 9
P: 2
R: 4
TT 6years, male FS: 75 [70, 82]
V: 64 [59–74]
P: 93 [87, 100]
S: 27
C: 22 (V)
13 (NV)
R: 8
Onset: 4
Module 1
C: 8
S: 10
P: 0
R: 2
ET 8years, male FS: 59 [55, 66]
V: 59 [55, 69]
P: 65 [60, 74]
S: 28
C: 18 (V)
14 (NV)
R: 8
Onset: 4
Module 2
C: 7
S: 14
I: 2
R: 6
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2094 Journal of Autism and Developmental Disorders (2018) 48:2090–2100
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modulating EEG mu rhythms by the progression of video
games or by an increase in the size of the display screen
playing preferred DVD movies. The acoustic marker was
also incorporated into the neurofeedback software and was
heard when thresholds were met.
Results
General Feasibility ofTAGteach
Results are summarized for all seven cases regarding the
use of TAGteach to train prerequisite skills, and facilitate
MSI testing and NFT. Individual case details are presented
thereafter.
TAGteach‑Assisted Behavioral Preparation
At baseline, participants met behavioral criteria for an aver-
age of 12.6 (± 3.8) items, or 49%, of the 26-item task analy-
sis; all cases had difficulty tolerating the skin preparation
procedures and/or electrode placements, and all were unable
to sustain the prerequisite skills for their required durations
of 120s. Following an average of 5.0 (± 1.0)h of TAGteach
intervention over 5.9 (± 1.2) training sessions, six partici-
pants demonstrated 100% and one demonstrated 92% of
behavioral criteria identified in the task analysis (see Fig.1).
Learning was initially facilitated by tagging parents or a
toy doll, or by first using a dry swab or water instead of the
skin preparation gel. We used the value-added tag point to
“Dry off” the preparation gel. During training, three cases
had more difficulty progressing in visually attending to the
non-biological motion video of an oscillating shape of a cir-
cle, presumably because of a lack of interest in the content.
Adding another video stimulus of more interesting content,
a train moving along a railroad, was successful in facilitating
progress. All cases needed an occasional verbal prompt in
one or more of their discrete trials when learning to sustain
behaviors for 120s.
TAGteach‑Assisted Mu Suppression Testing
TAGteach facilitated the participation in MSI testing for
all seven cases. Each case demonstrated artifact-creating
behaviors during part of one or more MSI testing tasks, for
instance, speech, noncommunicative vocalizations, fidg-
eting, or biting or licking the chin rest. During the action
execution task, two participants executed the hand motion
with a notably variable pace and size of the grasping com-
pared to learning trials, two exhibited some unusual hand
or finger mannerisms, and one ceased the motion entirely
without resuming after verbal prompts. Five cases had dif-
ficulty attending to the action observation videos, and verbal
prompts were provided at the clinician’s discretion; one case
peered out of the corner of her eye. Three cases commented
on or imitated the actions observed in the videos upon stimu-
lus presentation, potentially related to the novelty of video
stimuli presented during MSI testing relative to the stimuli
used to train visual attention, a feature that was not consid-
ered when creating the task analysis of prerequisite skills. At
post- and follow-up testing, it was necessary to reshape the
self-generated hand motion using TAGteach for four cases.
TAGteach‑Assisted Neurofeedback
TAGteach facilitated participation in NFT for all seven
cases. Over 23 (± 4) weeks, participants completed a mean
of 17.5 (± 3.4)h of NFT over 36.3 (± 7.0) sessions. Neuro-
feedback training segments were kept shorter at first, then
gradually lengthened up to 10min. Upon the introduction
of NFT, four cases seamlessly and immediately engaged in
NFT. Three cases had difficulty engaging in NFT upon treat-
ment introduction for the required 30min per session, but
TAGteach was successfully used to assist these individu-
als to engage in NFT in gradually increasing durations (see
Fig.2).
RC
RC is a 7year-old male with a history of seizures and
significant difficulties with aggression, anxiety, and inat-
tention. Though he was able to demonstrate sitting still
and quietly, he made odd facial expressions at times so
he earned tag points for relaxing his muscles. He was
observed to engage in increasing hand-flapping behavior
while learning the self-performed hand motion, presum-
ably due to focus fatigue; thus, we ended this session at
Fig. 1 Percent behavioral criteria met across TAGteach sessions rela-
tive to baseline
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a point of success and hand-flapping was not problematic
when he resumed training in his next session.
CR
CR is a 6year-old male with a history of marked hyper-
activity and disruptive behavior, and a tendency to be
oppositional, noncompliant, and destructive. Other chal-
lenging behaviors included frequent screaming; crying;
repetitive vocalizations; aggressive outbursts; and compul-
sive or stereotyped behaviors. He made frequent demands
to alter the behavior of the experimenter or the environ-
ment, and when reasonable, his preferences were accom-
modated. Though CR already demonstrated tolerance of
sensor placement at baseline, he was unwilling to do so
after commencing TAGteach training. He had difficulty
performing the hand-movement, preferring to use his left
or both hands. His willingness to perform the hand move-
ment correctly was contingent on being allowed to earn
tag points for performing it with his other hand. In accord
with TAGteach philosophy, we strongly emphasized the
offering of choice to CR to help address his tendency
to demand control and compulsively complete specific
behavioral sequences.
During NFT, disruptive behaviors included unplugging
electrodes and equipment power cords, removing sensors,
and expressing displeasure for sounds or elements within
NFT scripts. After minimizing access to lab equipment
and environmental distractions, TAGteach was used to
shape his ability to engage in NFT in increasingly longer
training segments. We also individualized some NFT
scripts, and made more neurofeedback games available to
increase his interest.
SR
SR is a 7year old female who has shown limited response
to traditional behavioral therapies. She is suspected to have
a seizure disorder which has never been confirmed due to
her inability to tolerate EEG testing. She is known to display
trichotillomania behaviors when under increasing stress;
thus, her sessions were kept short to avoid focus fatigue and
discontinued if she displayed any signs of hair-pulling. She
named the tag point for performing the skill of quietly sitting
motionless, “Sit like a statue.” Despite past intolerance of
EEG testing, SR learned all required behaviors after 4h of
TAGteach training.
ZB
ZB is a 7year-old male whose challenging behaviors include
tantrums and aggressive outbursts. His willingness to toler-
ate sensor placements was at times dependent on earning
tag points for attaching the electrodes himself. The experi-
menter also assigned a tag point to “leave wires on” to fade
ZB’s behavior of removing sensors between each trial. When
training the hand movement, ZB required the experimenter
to verbally count down till the task was completed. The use
of an audio/visual timer ameliorated this by gradually mov-
ing it out of view across discrete trials.
XD
XD is an 8year-old male who presented with avoidant and
self-injurious behaviors, hyperacusis, tantrums, sensory
hypersensitivities, and frequent insistence on sameness. He
often avoided sitting down or the experimenter by leaving
the room or building. After noting that avoidant behaviors
increased following approximately 40min of TAGteach, we
structured sessions to be shorter. When training to sustain
visual attention to stimuli while wearing sensors, he first
tagged his doll to do so, then he tagged himself, and subse-
quently allowed his mother and then the experimenter to tag
him. XD had difficulty engaging in NFT upon introduction
as evidenced by removing electrodes. TAGteach facilitated
his ability to engage in NFT in increasingly longer durations.
SK
SK is a 6 year-old male whose challenging behaviors
included hyperactivity, hyperacusis, inattention, anxiety
and obsessive–compulsive symptoms. SK learned to per-
form 92% of behavioral criteria following 6h of TAGteach
over six sessions. He learned sufficient skills to participate in
NFT through TAGteach but was unable to adequately sustain
Fig. 2 Minutes of neurofeedback completed per session. Note the
reduction in minutes of neurofeedback completed for session 31–32
of case CR was due to equipment
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2096 Journal of Autism and Developmental Disorders (2018) 48:2090–2100
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all behaviors for the full 120s, though an attempt was none-
theless made to administer MSI testing by offering verbal
reminders of the current tag point as needed.
TT
TT is a 6year-old male with anxiety, frequent tantrum
behavior, and small bowel disease who tends to communi-
cate nonverbally before resorting to verbal communication.
His mother was heavily involved in skill teaching. Reinforce-
ment items that were highly desirable to TT were distracting
to his learning, and his selection of primary reinforcers was
limited by dietary restrictions. Individualized phrasing of
tag points was necessary for him to cooperate, for instance,
he refused to execute the hand motion with the phrasing,
“Open close hand,” but agreed after he suggested the modi-
fication, “Open shut hand.” His ability to perform the hand
motion deteriorated mid-training and he was reshaped to
execute the movement through the use of physical aid first,
through imitation next, and ultimately, independently. One
session was terminated early due to TT becoming so dis-
tressed due to difficulty communicating a choice preference.
We also removed the auditory marker from NFT scripts,
which resolved avoidant behaviors (e.g. covering his ears or
humming) likely related to hyperacusis. TT lost his ability to
execute the hand movement task at post- and follow-up MSI
tests so the behavior was reshaped via TAGteach.
ET
ET was an 8year old male who, similar to his brother TT,
had an extremely restrictive diet, small bowel disease, and
anxiety that required close involvement of his mother during
TAGteach training. He was withdrawn from the study due
to an exacerbation in gastrointestinal symptoms after two
TAGteach sessions. Relative to baseline, he showed progress
in learning to tolerate all skin preparation procedures and
sensor placements, cease vocalizations, and quietly sit still
for 30s. Sessions lasted 30min since his interest in primary
reinforcers after this amount of time declined. Though ET
was withdrawn early from the study, he did show learning
during TAGteach training and his case contributes to high-
lighting the difficulties in studying and treating children with
autism and more severe functional deficits.
Discussion
Investigating the feasibility of using TAGteach methodol-
ogy to behaviorally prepare intellectually-impaired children
with autism to undergo MSI testing and NFT resulted in
three main findings. TAGteach was a viable method for (1)
training behavioral criteria identified in a task analysis as
required to participate in NFT and MSI testing, (2) facilitat-
ing task performance during the MSI, and (3) facilitating
participant engagement in NFT.
Findings suggest that applied behavioral analytic meth-
odology that uses conditioned auditory reinforcers, or
TAGteach, is a feasible method for preparing children with
autism who lack skills necessary for a particular research or
clinical intervention to successfully participate. Our results
converge with the literature on classical and operant learning
in animals (McSweeney and Murphy 2014; Neuringer 2002)
and a small body of case report research on TAGteach with
humans and those with autism (see Pineda etal. 2014a)—
albeit accelerated learning was not examined in this study.
Theoretically, the use of conditioned reinforcement is con-
sistent with learning paradigms as simple as Pavlovian con-
ditioning or a rat in a Skinner box, and the widely accepted
effects of auditory reinforcers on animal learning and
behavior could feasibly be extended to facilitate learning in
children with greater autism severity. TAGteach may serve
as a practical tool for clinicians, researchers, parents and
teachers for enhancing independent functioning and access
to promising treatments. Rates of research study participa-
tion for individuals in the lower functioning range of the
autism spectrum also have the potential to be enhanced by
TAGteach.
Since commencing our study, Persicke etal. (2014) used
a modified TAGteach procedure to correct toe-walking in
a 4year-old male with autism. Using an ABAB design,
they examined: (a) Correction alone (i.e. gently push-
ing downward on the child’s shoulders), and (b) Correc-
tion + TAGteach (reinforcing correct steps). Correct foot-
steps were observed at a mean rate of 24.6% at baseline,
63.6% in the Correction Alone phase, and 90.5% in the Cor-
rection + TAGteach phase. A visual inspection showed that
correct steps clearly reduced in the reversal phases, and were
maintained above a rate of 73% in the fading and generaliza-
tion phases. Although promising, more research is needed to
determine if TAGteach can assist other children with autism
to reduce toe-walking behavior or other impairments. This
peer-reviewed case study is congruent with our results that
show TAGteach facilitates learning and provides additional
support by showing a powerful reversal effect.
Even though our participants demonstrated the ability to
sustain the four core skills during shaping procedures, our
results indicate that this requirement was not sufficient to
procure the level of mastery needed for reliable skill dem-
onstration during MSI testing, as several artifact-creating
behaviors were documented in multiple recording trials.
This was more problematic for action observation trials,
which could only be administered a single time whereas
we restarted EEG recording trials during resting baselines
and motor tasks if necessary. Herein, we discuss possibili-
ties to address limitations related to training this population
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through a combination of TAGteach and more advanced
methods of artifact-identification and technology usage,
principally biofeedback.
Limitations andFuture Directions
Future researchers using TAGteach ought to consider devel-
oping a sham or replica protocol of actual outcome test-
ing tasks and stimuli for assessing participant readiness to
undergo actual testing, identifying probable artifact-creating
behaviors that may need to be (re)targeted with TAGteach,
and identifying an acceptable level of behavioral and elec-
trophysiological artifact in data samples. For example, it is
more likely we would have pre-identified the problematic
effect of novelty in stimulus presentation had we performed
mock testing of the MSI, preempting the inclusion of a wider
variety of visual content when training subjects to complete
action observation trials. Mock testing conditions would also
aid future investigators in developing a thorough task analy-
sis prior to commencing shaping procedures.
One limitation of this study was the poor means of train-
ing sustained visual attention, which was subject to clinical
judgement. In future studies, stimuli content of a moderate
interest level should be elected for optimum results, as too
low a level of interest appeared to disengage participants,
and content with too high of a reinforcement value was dis-
tracting. Another means of verifying visual attention may
be to include an attention or counting task (see Pineda etal.
2008), albeit developing a uniform attention task that is
appropriate to all participants may be challenging given the
heterogeneity in cognitive and language abilities typical of
children who are low-to-mid range functioning. Neverthe-
less, the creative flexibility inherent in the TAGteach meth-
odology may allow the successful shaping of participant
ability to count and communicate the events of an attention
task, whether verbally or through a picture-communication
or computer-based program, or some other means. What is
more important is that more advanced software integrations
have the potential to not only help improve participant com-
munication through game-like user interfaces, but also to
enhance interest and motivation levels by rewarding their
cooperation, and perchance successively, their accuracy.
TAGteach may be a viable candidate to facilitate this sort of
research in lower functioning populations, ideally, in con-
junction with gaze tracking technology or other means of
enhanced artifact rejection.
Duffy and Als (2012) reported that they facilitated com-
pliance with EEG protocols in a group of children with low
functioning autism by using technologists experienced in
the special management of pediatric populations. Their
study posits that more sophisticated artifact-rejection and
unspecified behavior management techniques coupled with
relaxation breaks is sufficient to maintain a relatively low
level of EEG artifact in children with autism who are less
than high functioning—highlighting that conditioned audi-
tory reinforcers may not be a requirement. Alternatively,
the comparability of their study population to the present
one is weakened since they did not clarify their criteria for
low functioning autism or use standardized diagnostic or IQ
assessments, and instead relied on subjective diagnoses of
independent clinicians.
TAGteach may be able to assist in other methods for com-
pensating for group-specific artifact or skill deficits during
outcome testing, for instance, training participants to toler-
ate additional sensors. Technological advances in equipment
that minimize the participant or instructor demands and the
behavioral criteria needed for task compliance are also rec-
ommended, such as using a cap with dry leads or wireless
sensors. Lastly, as some cases had difficulty sustaining or
entirely ceased skill demonstration during some of the task-
related EEG trials, researchers may consider developing
formal criteria to determine when or if a discrete trial may
be restarted or if a uniform reminder of the present tag point
can be given and then sourced out during data analyses.
A more innovative extension of this study would be to
integrate biofeedback into TAGteach procedures for shap-
ing prerequisite skills, which could be useful for training
actions with greater specificity or for sustaining skill dem-
onstrations. For instance, a learner could receive real-time
auditory feedback about their muscle movement or visual
attention, which must be maintained above a predetermined,
cumulative threshold in order to earn a tag point at the end of
a discrete trial. A biofeedback-assisted TAGteach approach
such as this for shaping sustained skill demonstrations would
help resolve problems associated with depending on a sin-
gle auditory marker to mark the completion of performing
the skill at the end of a discrete trial, which unintentionally
reinforces behaviors that increase artifact even if they only
occur to a minor degree. Furthermore, customizable soft-
ware with multimedia capabilities, with which participants
can interact, may be useful in enhancing their communica-
tion about events and choosing preferred rewards, increasing
their interest and motivation to comply with task require-
ments. The feasibility of integrating biofeedback approaches
into TAGteach for shaping skills, particularly prolonged
skill demonstrations, is encouraged to continue carving a
path toward including more lower functioning children with
autism in more rigorous neuroscientific studies or behavioral
interventions.
Lastly, we recommend starting neurofeedback treatment
with lower functioning autism populations by selecting
shorter NFT segments (i.e. an estimate of 2–5min) inter-
spersed with breaks to improve the generalization of skills
from TAGteach training to NFT. Practitioners may opt to
use novel NFT games or movies rather than participants’
preferred DVD movies to minimize the chance that they will
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2098 Journal of Autism and Developmental Disorders (2018) 48:2090–2100
1 3
disengage due to psychological distress about familiar movie
content functioning in a different way than it has in their
other environments. More broadly, TAGteach could be of
use to some laboratories studying low- and high-functioning
children that are designing interactive environments (e.g.
video-games, e-learning applications, virtual realities) with
neurofeedback-integration capabilites to optimize electro-
physiological activity and reward desired behavior in direct
correspondence with the underlying significance of per-
ceived stimuli (for instance, see Friedrich etal. 2014).
Regarding the aforementioned suggestions, TAGteach
appears worthy of further exploration to determine if it can
prepare more highly-impaired individuals with sufficient
skills to comply with treatment and research tasks, and if
the method can be supplemented in research studies by more
sophisticated means of electrophysiological measurement,
computational, or artifact rejection techniques; technological
advances in human–computer interfaces; or other individual-
ized, teaching adaptations. Findings from the present case
series begin to impart support for TAGteach as a means of
exploring whether the prerequisite skills of such adaptations
to research and teaching methods can be successfully incor-
porated into TAGteach training.
As in all single-subject research, the effects of TAGteach
cannot be causally determined from the present design.
Without independent raters, TAGteach findings were bound
to the sole judgment of the experimenter. Additionally, the
nonrepresentative sample used in the current case series
restricts the external generalizability of case results.
Conclusions
This case series shows that it is feasible to use conditioned
auditory reinforcers to teach intellectually-impaired chil-
dren with autism to cooperate with a neurofeedback study
and task-dependent EEG outcome tests. However, research
is still needed to determine (a) if TAGteach is preferable
to other teaching methods, (b) if TAGteach can facilitate
improved skill performance during EEG outcome testing or
NFT, and (c) whether incorporating skills required of more
demanding or rigorous research methods into TAGteach
training is a viable means of improving skill generalization
to treatment and outcome measure tasks. Unquestionably,
intellectually-impaired children with autism are deserving of
a greater rate of inclusion in treatment and other studies by
developing empirically-supported, skill-teaching methods to
improve their participation. TAGteach appears to be a candi-
date to help amend this problem—warranting further study.
Acknowledgments Thanks to Yvonne Searcy and Theresa McKeon
for their assistance in training the instructors to implement TAGteach.
Author Contributions All authors contributed to the research design,
data analyses and interpretation, and writing and preparing of the man-
uscript. KL conducted the diagnostic assessments, TAGteach training,
and data collection. AL supervised the diagnostic testing. All authors
read and approved the final manuscript.
Compliance with Ethical Standards
Conflict of interest The authors disclose no conflicts of interest.
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