Motor Skill in Autism Spectrum Disorders: A Subcortical View

CHAPTER SEVEN
Motor Skill in Autism Spectrum

Disorders: A Subcortical View
Leanne Chukoskie*,1, Jeanne Townsend†, Marissa Westerfield*
*Institute for Neural Computation, University of California, San Diego, California, USA
†
Department of Neurosciences, University of California, San Diego, California, USA
1
Corresponding author: e-mail address: lchukoskie@ucsd.edu
Contents
1. Why Study Motor Skill in Autism? 208
1.1 Motor skill as foundational in development 209
1.2 Early signs are motor 210
1.3 Correlation with social and communication skill 211
2. Overview of Motor Skill Deficits 212
2.1 Gross motor skills 212
2.2 Fine motor skills 215
2.3 Dyspraxia 216
2.4 Eye movements 217
3. Mapping Autism Motor Skill Findings into a Useful Framework 218
3.1 Cortico–subcortical loops for motor control 218
3.2 How do autism motor skill deficits fit in this framework? 225
4. Can We Intervene? 228
4.1 Motor skill training in rodents 230
4.2 Motor training for children with ASD? 232
4.3 Motor training for older adults with ASD? 233
5. Summary 234
References 235
Abstract
The earliest observable symptoms of autism spectrum disorders (ASDs) involve motor
behavior. There is a growing awareness of the developmental importance of impaired
motor function in ASD and its association with social skill. Compromised motor function
requires increased attention, leaving fewer resources available for processing environ-
mental stimuli and learning. This knowledge suggests that the motor system—which
we know to be trainable—may be a gateway to improving outcomes of individuals liv-
ing with ASD. In this review, we suggest a framework borrowed from machine learning
to examine where, why, and how motor skills are different in individuals with ASD.
International Review of Neurobiology, Volume 113 # 2013 Elsevier Inc. 207

ISSN 0074-7742 All rights reserved.
http://dx.doi.org/10.1016/B978-0-12-418700-9.00007-1
208 Leanne Chukoskie et al.
1. WHY STUDY MOTOR SKILL IN AUTISM?

Autism is a behaviorally defined disorder characterized by deficits in
social engagement, atypical verbal and nonverbal communication, and a
focus on ritualized behaviors and restricted interests. Despite its absence
from diagnostic criteria, differences in motor skills in individuals with autism
spectrum disorder (ASD) have been observed from the earliest descriptions
of the disorder (Kanner, 1943).
In his landmark 1943 description of autism, Leo Kanner noted uneven
motor development, including clumsy gait and gross motor performance, in
a few of the 11 cases he described. Kanner also reported that many of the
mothers of these children noted with surprise that the infants failed to
“assume at any time an anticipatory posture preparatory to being picked
up” and even at 2 or 3 years of age failed to adjust their bodies to the posture
of the person holding them—something typical infants do by 3 or 4 months
of age (Kanner, 1943).
Hans Asperger reported motor clumsiness in all four of the case studies he
presented in his initial 1944 paper (Asperger & Frith, 1991). As did Kanner,
Asperger noted both gross and fine motor abnormalities; for example, he
remarked that “atrocious handwriting” (due to an inability to control the
pen) was a common trait in most autistic individuals. A more evocative
description of the flavor of motor impairments is found in observations of
a child known as “Harro L.”:
His movements never unfolded naturally and spontaneously. . .from the proper
co-ordination of the motor system as a whole. Instead, it seemed as if he could
only manage to move those muscular parts to which he directed a conscious effort
of will. (p. 57)
Asperger pointed out that when trying to understand the difficulty autistic
children had in learning practical, everyday skills, it was impossible to tease
apart motor clumsiness from lack of understanding and believed that the two
deficits were in fact linked.
As the ASDs are considered as part of a larger collection of neu-
rodevelopmental disorders, it might be expected that cooccurring neurolog-
ical symptoms are common and both eye and body movement deficits
would fall in this category. However, several studies suggest that motor skill
deficits may be central to our current conception of ASD (Fournier,
Hass, Naik, Lodha, & Cauraugh, 2010; Hilton, Zhang, Whilte, Klohr, &
Constantino, 2012; Mostofsky and Ewen, 2011). In ASD, the symptoms
Motor Skill in Autism Spectrum Disorders 209
frequently observed include motor skill delays, deficits, and atypical move-
ment patterns (Fournier, Hass, et al., 2010; Jansiewicz et al., 2006; Maski,
Jeste, & Spence, 2011). Children with ASD showed greater impairments
in motor skill on a standardized motor testing battery when compared to
children diagnosed with other neurodevelopmental disorders (Dewey,
Cantell, & Crawford, 2007). The children with autism were also the only
group to show impairments in gestural skills. An insightful recent study of
Hilton and Constantino (Hilton et al., 2012) examined the performance
of 83 sibling pairs, some concordant and some discordant for autism, using
a comprehensive and standardized motor skill battery and found that motor
performance was strongly correlated with the diagnostic status but not with
sibship. The authors argue that given the highly heritable nature of ASD,
this finding suggests that motor measures should factor into the diagnosis
of autism.
1.1. Motor skill as foundational in development

From early in development, children use both fine and gross motor skills to
indicate wants and needs. Bushnell and Boudreau (1993) summarized the
perspective that motor skills establish a developmental plan or “timetable”
for development in other domains. For example, gestures in infancy appear
to pave the way for later language use (Iverson & Goldin-Meadow, 2005).
A recent research suggests a model in which early motor exploratory behav-
ior, such as learning to reach, serves as a scaffold for later prosocial-looking
behaviors (Libertus & Needham, 2010). A case in point is a novel study of
motor control in young infants that demonstrated advanced development of
social skills in babies who wore “sticky mittens” that allowed them to grasp
and control objects that they could not otherwise reach or grasp (Libertus &
Needham, 2010). A large study of typical development found that better
motor function in early infancy was associated with better development
of language and nonverbal cognition at 2–3 years of age (van Batenburg-
Eddes, Henrichs et al., 2013). Further, a study of school readiness in typical
kindergarten children found that fine motor skills and attention were pre-
dictors of later academic achievement (Grissmer, Grimm, Aiyer,
Murrah, & Steele, 2010).
An evidence for the association of motor function and social and cogni-
tive development also comes from studies of developmental motor disor-
ders. A study of 122 toddlers with cerebral palsy found a strong
relationship between motor skills and social development (Whittingham,
Fahey, Rawicki, & Boyd, 2010). Taken together, these studies suggest that
one might consider atypical motor development as a critical factor in the
further development of symptoms that characterize autism in children aged
two and older.
1.2. Early signs are motor

By examining home movies for infants later diagnosed with ASD,
Teitelbaum and colleagues noted frequent atypical motor milestones in
addition to the occurrence of atypical mouth postures, lateral asymmetries,
and failures in the reflexive preparation to brace for a fall (Teitelbaum et al.,
2004; Teitelbaum, Teitelbaum, Nye, Fryman, & Maurer, 1998). Baranek
(1999) coded sensorimotor behaviors in videos of 9- to 12-month-old
infants in three groups: those who were later diagnosed with autism, those
later diagnosed with a developmental delay, and those with typical develop-
ment. Infants who were later diagnosed with autism exhibited a higher fre-
quency of unusual postures, atypical orienting, and object-directed
behaviors and atypical responses to the infant’s own name and social touch.
Some have questioned whether the differences observed from the retrospec-
tive video are more indicative of delays and not true deficits in ASD
(Ozonoff et al., 2008), but others have shown that atypical motor skill per-
sists through adolescence and adulthood (Glazebrook, Elliott, & Szatmari,
2008; Nazarali, Glazebrook, & Elliott, 2009; Perry, Minassian, Lopez,
Maron, & Lincoln, 2007; Travers, Powell, Klinger, & Klinger, 2013;
Weiss, Moran, Parker, & Foley, 2013). Hypotonia (51%), dyspraxia
(34%), and toe walking (19%) were the most common motor symptoms
found in a retrospective clinical neurological record review, with both
hypotonia and dyspraxia being more common early in development
(Ming, Brimacombe, & Wagner, 2007).
When researchers began to prospectively examine baby siblings of indi-
viduals with ASD in early infancy, who tend to be diagnosed with autism at a
higher rate than the general population (18.7% recurrence according to a
recent study; Ozonoff et al., 2011), the researchers noted that the very first
signs of atypical development were motor. In 2005, Zwaigenbaum and col-
leagues and others (Landa & Garrett-Mayer, 2006; Ozonoff et al., 2010;
Zwaigenbaum et al., 2005) reported early signs observable in baby siblings
who go on to develop autism. Deficits were observed in orienting behavior
including atypical eye contact, social smiles, visual tracking, and orienting to
the child’s own name and in the timing and disengagement of fixation. More
recently, Landa and colleagues (Flanagan, Landa, Bhat, & Bauman, 2012)
reported that 6-month-olds at high risk for ASD had more head lag when
pulled up to a seated position. Both Ozonoff et al. (2010) and Landa and
Garrett-Mayer (2006) observed an increasing trend toward atypicality
between the first and second year, with gross and fine motor differences
in the high-risk ASD siblings emerging in one study (Landa & Garrett-
Mayer, 2006) that measured them. High- and low-risk infants were not sta-
tistically distinguishable by motor skill differences at 6 months, but over
the following 8 months, low- and high-risk groups became more distinct.
At 24 months, the ASD-diagnosed group also differed in motor skill from
children who were diagnosed with language delay.
It also appears that early motor skill development is a strong predictor of
ASD outcome in later childhood. Sutera et al. (2007) reported that motor
skills at 2 years old were the best predictors of outcome in ASD at 8 years
old. This is an important research that needs further study, as there are very
few solid predictors of outcome in ASD.
1.3. Correlation with social and communication skill

Although poor motor coordination was a part of the original descriptions of
ASD, specific aspects of motor skill deficits and the implications of these def-
icits for cognitive and social function have only recently begun to receive
attention. Several studies have shown that the level of motor impairment
is correlated with the level of social impairment in individuals with ASD
(Dziuk et al., 2007; Haswell, Izawa, Dowell, Mostofsky, & Shadmehr,
2009; Hsu et al., 2004; Moruzzi, Ogliari, Ronald, Happe, & Battaglia,
2011). Communication delays were present in approximately 70% of the
siblings of individuals with ASD who also showed early motor delays
(Bhat, Galloway, & Landa, 2012). One could imagine how impaired early
motor development could derail the development of social communication
as the building blocks of joint attention include appropriately timed gesture
and gaze-following.
In addition, data showing the tightly bound interaction of attention and
motor function suggest that compromised motor function requires increased
attention, leaving fewer resources to process and learn (Cherng, Liang,
Chen, & Chen, 2009; Huang & Mercer, 2001; Laufer, Ashkenazi, &
Josman, 2008; Tsai, Pan, Cherng, & Wu, 2009). Despite the growing evi-
dence that underscores the importance of early motor behavior that scaffolds
later social skills in typical development (Libertus & Needham, 2011), this
remains an understudied domain in ASD and we are only beginning to

understand the possible origins of atypical motor behaviors in ASD
(Greffou et al., 2012; Haswell et al., 2009). The impact of motor perfor-
mance on attention has also been observed in other disorders such as devel-
opmental coordination disorder (DCD) (Laufer et al., 2008; Tsai et al., 2009)
and cerebral palsy (Reilly, van Donkelaar, Saavedra, & Woollacott, 2008).
2. OVERVIEW OF MOTOR SKILL DEFICITS

Generalized motor deficits are common in ASD, but we lack a body of
quantitative, model-driven studies yielding specific results tied to the mech-
anism. Clinical studies with a neurology focus have a rich history of using neu-
rological “soft signs” to assess motor skill deficits (Haas et al., 1996). Although
these tests have been quite useful for diagnostic purposes and have highlighted
the generalized motor deficits of individuals diagnosed with autism, they have
not been as useful for research studies aimed at quantifying types and levels of
motor impairment. For this purpose, normalized, comprehensive motor tests
permit motor skill evaluations in an age- and sex-specific manner. When tests
like these are used, they reveal that motor deficits in autism encompass gross
and fine, static and dynamic, and simple and complex. Note, however, that in
several studies, lower intellectual ability seems to be related to poorer motor
skill across many tasks (Mostofsky et al., 2006).
2.1. Gross motor skills

We review results of research suggesting deficits in three gross motor skills in
individuals with ASD. Although we have discussed results as generic to ASD,
there is a tremendous amount of heterogeneity in the presentation of the
disorder—motor skill included. Some researchers, notably Rinehart and col-
leagues, have made a point of noting larger gross motor deficits in individuals
with autism than in individuals with Asperger’s syndrome (Nayate et al.,
2012). But as others have not found differences between these groups
(Ghaziuddin & Butler, 1998; Ghaziuddin, Butler, Tsai, & Ghaziuddin,
1994; Jansiewicz et al., 2006; Manjiviona & Prior, 1995) and recent studies
question our ability to reliably distinguish between these diagnostic categories
(Lord et al., 2012), we will describe the results together. In fact, in the latest
version of the Diagnostic and Statistical Manual (V), Asperger’s syndrome is no
longer listed as a diagnosis (Association, A. P., 2013).
2.1.1 Balance
Balance deficits have been measured using scientific grade force plates across
a wide age range of individuals with ASD and normal intelligence (Chang,
Wade, Stoffregen, Hsu, & Pan, 2010; Fournier, Kimberg, et al., 2010;
Kohen-Raz, Volkmar, & Cohen, 1992; Minshew, Sung, Jones, &
Furman, 2004; Molloy, Dietrich, & Bhattacharya, 2003). In an early study
from Minshew et al. (2004), the impairments were most pronounced in con-
ditions that perturbed either visual (eyes closed or sway-referenced sur-
roundings) or somatosensory stimulation (sway-referenced platform).
Recently, Travers et al. (2013) demonstrated impaired balance in adoles-
cents and adults with ASD using the low-cost Wii Balance Board
(WBB), which has been favorably evaluated with respect to the scientific
grade force plate (Clark et al., 2010; Huurnink, Fransz, Kingma, & van
Dieen, 2013), had excellent test–retest reliability, and performed better than
the widely used Balance Error Scoring System (Chang, Levy, Seay, & Goble,
2013). Here too, individuals were found to have impaired balance under
“challenged” conditions, in this case while standing on one leg.
2.1.2 Gait
Static and dynamic balance skills are essential to functional gait performance.
Balance skill reflects sensorimotor status through the complex integration of
sensory feedback and coordinated motor responses to keep one’s center of mass
over the body’s base of support. Several studies of gait have reported atypical
gait in individuals with ASD. Qualitative evaluations have revealed a lack of
smoothness or overall coordination, atypical trunk and arm postures, or asym-
metrical gait (Esposito, Venuti, Apicella, & Muratori, 2011; Hallett et al., 1993;
Rinehart et al., 2006; Shetreat-Klein, Shinnar, & Rapin, 2012). Quantitative
evaluations have confirmed the lack of smoothness and irregular trunk move-
ments and in addition have shown significant differences in other spatial and
temporal gait parameters (Nobile et al., 2011; Vernazza-Martin et al., 2005;
Vilensky, Damasio, & Maurer, 1981; Weiss et al., 2013). While the specific gait
parameters identified as abnormal vary from study to study, shorter step/stride
length in ASD is a common finding. Atypical gait might result directly from
difficulties in balance (Lajoie, Teasdale, Bard, & Fleury, 1993), although hypo-
tonia may also play a role (Calhoun, Longworth, & Chester, 2011).
2.1.3 Reaching
There are relatively few studies of true reaching behavior in ASD; however,
several findings bear on reaching. Children with ASD appear to be slower in
performing anticipatory postural adjustments, such as one would make to grab

or let go of a heavy object (Schmitz, Martineau, Barthelemy, & Assaiante,
2003). Children with ASD also failed to anticipate making a hand movement
that was very predictable—a departure from what is observed in typical chil-
dren (Rinehart et al., 2006). However, the failure of this movement is likely in
the anticipation, not in the ability to execute the movement. Mon-Williams
and colleagues (van Swieten et al., 2010) showed that adolescents with ASD
performed a single hand-turning movement in a manner similar to their typ-
ically developing age-matched peers. The distribution of starting and ending
hand postures was normal in autism but very atypical in children with DCD.
Several studies suggest deficits in sequential reach planning for individuals
with ASD. Cattaneo and colleagues (Cattaneo et al., 2007) measured electro-
myography (EMG) responses of the mouth-opening muscle during a two-
step movement involving picking up a small item and placing it either in a
cup secured to the shoulder or in the mouth. A food item indicated that
the target was the mouth, and a small paper ball indicated that the movement
should be to the shoulder cup EMG. Typically developing children showed
EMG evidence of preparation for food arrival at the mouth at least 1 s in
advance of grasping the piece of food to move it to the mouth. Children with
ASD did not show any mouth-opening EMG activity until the food was
grasped. In a follow-up experiment (Fabbri-Destro, Cattaneo, Boria, &
Rizzolatti, 2009) that required children to pick up an object and then reach
to place it in either a small or large cup, children with ASD did not show evi-
dence in their first movement of the plan required for the second movement.
These studies illustrate a lack of integration of movements that compose a
sequence, and importantly most movements are not singular but executed
as part of a sequence.
Both the anecdotal reports and the few studies of arm movement
trajectory reveal variability in the movement itself (Glazebrook, Elliott, &
Lyons, 2006; Glazebrook, Gonzalez, Hansen, & Elliott, 2009; Mari,
Castiello, Marks, Marraffa, & Prior, 2003). This is interesting since reaching
movements are typically very repeatable both within and across subjects.
One suggestion for the degree of variability has been the injection of noisy
or biased sensory feedback into the movement. Several studies have asked
how vision and proprioception contribute to reaching in ASD.
Glazebrook et al. (2009) found longer duration and more variable
movements when vision was normal versus when it was occluded at the
launch of the movement, suggesting that visual guidance was somehow
problematic. Mari et al. (2003) showed differences in timing of a
reach-to-grasp movement that varied with intellectual ability in a sample of

20 children with ASD, with children who had the lowest IQ ranges also hav-
ing the slowest, almost parkinsonian movements. The control children were
matched for age, intellectual ability, and handedness, yet did not share the
variance in movement quality and timing observed in the ASD group.
Mostofsky and colleagues conducted a quantitative and theory-driven
examination of the contribution of sensory feedback to a learned arm move-
ment in a novel force field environment (Haswell et al., 2009). In this and a
follow-up study comparing children with ASD to children with attention-
deficit/hyperactivity disorder (ADHD) (Izawa et al., 2012), the investigators
examined how the newly learned contingencies transferred when the arm
position was shifted toward the right. The pattern of movement trajectories
observed in the transfer suggested a greater reliance on proprioceptive input
over visual input (Haswell et al., 2009). Compared to children with ADHD,
children with ASD showed a pattern of generalization suggesting a greater
reliance on proprioceptive input (Izawa et al., 2012). These results were inter-
preted as possibly resulting from local overconnectivity in cortex, which has
been reported by other groups (Belmonte et al., 2004; Muller et al., 2011).
2.2. Fine motor skills

Fine motor skills have been studied most often as a part of larger motor skill
batteries and have recently been the focus of a number of investigations.
A large study of 10- to 14-year-old children with ASD reported that 79%
of the children showed fine motor skill deficits as part of the Movement
Assessment Battery for Children (Green et al., 2009). One report found that
gross and fine motor skill deficits were roughly equivalent in children with
ASD (Provost, Heimerl, & Lopez, 2007). Grasping is an important early
motor skill for an infant exploring his or her world. At school age, items
to manipulate become smaller and handwriting becomes increasingly nec-
essary, demanding improved fine motor control.
In a recent study examining precision grip, the researchers examined
temporal execution of grip onset with respect to load onset and peak grip
force. Both ASD and developmentally delayed groups had developmental
trajectories between ages 2 and 6 that differed in comparison with typical
children on two measures of grip timing, but not force (David, Baranek,
Wiesen, Miao, & Thorpe, 2012). These results suggest that problems with
timing patterns of action affect fine motor control in addition to other timing
problems in gross motor patterns, such as gait.
Illegible handwriting was specifically noted by Hans Asperger in his initial

description of this disorder (Asperger & Frith, 1991). Fuentes and colleagues
led a study of handwriting in individuals with ASD quantifying this observa-
tion, especially noting deficits in letter form quality, and reporting the corre-
lation to overall motor performance (Fuentes, Mostofsky, & Bastian, 2009).
Handwriting is interesting in that it requires more than just fine motor skill
but also visual perceptual and visuomotor-integration skill together with pro-
prioception (Kushki, Chau, & Anagnostou, 2011). Since various researchers
have reported consistently poor visuomotor integration (Fulkerson &
Freeman, 1980; Mayes & Calhoun, 2003), it is not surprising that handwriting
skill is particularly weak in individuals with ASD.
2.3. Dyspraxia
The term dyspraxia (or apraxia for the more severe form) refers to difficulty
in organizing, planning, or executing skilled movement, which impairs
movement fluidity and speed, and importantly is out of proportion to
any underlying motor deficits. Not surprisingly, this has been difficult to
assess clearly in ASD because the contribution of “underlying motor def-
icits” remains to be concretely characterized. What is that “something
extra” that is dyspraxia? Several batteries have been used to measure
impairment with the “conceptualization” of the movement (Weimer,
Schatz, Lincoln, Ballantyne, & Trauner, 2001). These batteries typically
include subtests to assess spatial orientation, movement selection and
sequencing, imitation, spontaneous tool use, limb kinetics, and oral–facial
skills. These batteries emphasize learned, purposeful movements that are
often performed as a sequence, and it is perhaps the motor sequence, which
is “something extra.” Using one of these test batteries, Mostofsky and col-
leagues reported lower levels of simple motor skill in addition to dyspraxia
(Dowell, Mahone, & Mostofsky, 2009). This suggests that there may be
deficits in both simple motor skill and the “something extra” that is
dyspraxia. Oral–motor dyspraxia such as difficulty in imitating mouth
shapes and noises or spontaneously producing them by name is relatively
common, and perhaps, it includes the failure of the incredibly complex
machinery of the mouth and tongue to engage both sequentially and in
concert in order to produce comprehensible speech (Belmonte et al.,
2013; Larson & Mostofsky, 2008). It is intriguing to consider how a deeper
understanding of oral–motor praxis could be translated to interventions for
those that are minimally verbal.
2.4. Eye movements

Studies of eye movement behavior are somewhat more developed than
other studies of motor behavior in autism, with many studies of eye move-
ments and attention potentially indicating failures of motor planning. Most
studies have focused on the social aspect of looking behavior (see, e.g., Klin,
Jones, Schultz, Volkmar, & Cohen, 2002; McPartland, Webb, Keehn, &
Dawson, 2011) but have neglected details regarding saccade metrics and
timing. A few studies that explicitly examined eye movement metrics during
standard visually guided target tasks have found increased variability in trial-
to-trial amplitude in the saccades of individuals with ASD (Johnson et al.,
2012; Luna, Doll, Hegedus, Minshew, & Sweeney, 2007; Takarae,
Minshew, Luna, & Sweeney, 2004). Other studies examined disengagement
of attention in addition to eye movement metrics (Elsabbagh et al., 2009;
Kawakubo et al., 2007; Landry & Bryson, 2004; Zwaigenbaum et al.,
2005). Although this literature is mixed, many studies find a hypometria
in the primary saccade that is often compensated by secondary or “correc-
tive” saccades (Johnson et al., 2012; Takarae et al., 2004). Since the refrac-
tory period is at least 100 ms, this inaccuracy is problematic in terms of
gathering information from dynamic scenes. A recent eye tracking study
of a magician’s performance suggests that these differences may hamper
an ASD individual’s ability to successfully collect information from a
dynamic environment (Kuhn, Kourkoulou, & Leekam, 2010). Over the
course of development, the accumulation of missed information can lead
to deficits in social and communicative behaviors.
The goal of a smooth-pursuit eye movement is to match the position
and velocity of a typically small moving target. These eye movements are
interesting to examine as they require accurate sensory estimation of target
velocity and an accurate motor plan incorporating initially an internal
model-based estimate of target error and later the actual target error.
Takarae, Minshew, Luna, Krisky, and Sweeney (2004) measured smooth-
pursuit eye movements in individuals with ASD and found lower velocity
during the later “closed-loop” phase of smooth pursuit and also lower veloc-
ity during the initial “open-loop” phase and hypometria in the initial catch-
up saccade, but only for rightward step-ramp target trajectories moving away
from the fovea. The closed-loop velocity deficit was the most robust for
older individuals with ASD, suggesting some sort of developmental matu-
ration that fails to occur in individuals with ASD. Importantly, no differ-
ences were found in the latency to initiate either pursuit or saccade.
There are many ways to mark eye movement latency and doing so can be
difficult in atypical eye movements. Since pursuit and saccade latency deficits
were expected given the other pattern of deficits and saccade latency delays
were observed elsewhere, it would be useful to see a replication of this result.
3. MAPPING AUTISM MOTOR SKILL FINDINGS

INTO A USEFUL FRAMEWORK
The cerebellum and basal ganglia each have different local circuit
architectures and synaptic learning mechanisms (Doya, 1999, 2000) that
are specialized for different types of information processing. We might best
approach an understanding of subcortical motor processing in ASD by ask-
ing what each area is specialized to learn. Motor skill learning and perfor-
mance are, of course, the integrated product of activity in multiple
cortical and subcortical brain regions. However, recent models of motor skill
learning from Doya and Hikosaka (Hikosaka, Nakamura, Sakai, &
Nakahara, 2002) clarify the particular importance of the basal ganglia and
cerebellum in optimizing motor skills during learning. Here, we review
results that suggest differences in function and connectivity in the basal gang-
lia and the cerebellum as they relate to motor skill in autism and place them
in the context of a larger framework of motor skill learning.
3.1. Cortico–subcortical loops for motor control

The anatomy suggests that both basal ganglia and cerebellum serve both
motor and nonmotor functions (for a review, see Bostan, Dum, & Strick,
2013). Both basal ganglia and cerebellum, through their feedback architec-
tures, are likely involved in optimizing motor skills during learning
(Hikosaka et al., 2002). Each area has unique computations and neither area
acts in isolation—it is the joint actions of these subcortical components along
with their cortical targets that support motor skill learning and the perfor-
mance of dexterous motor skill.
In the following two sections, we will describe what current modeling
(Doya, 1999, 2000) and experimental results (Houk & Wise, 1995)
have determined to be the canonical computations occurring in the
corticocerebellar and cortico-basal ganglia loops. Although our focus here
remains on motor skill learning and production, the neuronal machinery
of each subcortical area is likely performing the same sort of computation
for nonmotor functions.
3.1.1 Corticocerebellar loops

The cerebellum is commonly thought of as a motor coordination and con-
trol structure, though detailed anatomical tracing studies have revealed a
repeating pattern of loops through associative brain areas, including parietal,
limbic, and prefrontal cortices (Bostan et al., 2013), and a host of imaging
studies suggest that it is involved in processes beyond motor control and
coordination including attention (Allen, Buxton, Wong, & Courchesne,
1997; Kellermann et al., 2012; Le, Pardo, & Hu, 1998), working memory
(Durisko & Fiez, 2010; Hautzel, Mottaghy, Specht, Muller, & Krause,
2009), spatial processing (Fink et al., 2000; Stoodley, Valera, &
Schmahmann, 2012), and language (Desmond & Fiez, 1998; Schlosser
et al., 1998; Xiang et al., 2003). Returning our focus to the motor aspects
of the cerebellum, connections with primary motor cortex (M1) are best
known. However, the region of the dentate cerebellar nucleus that repre-
sents the arm appears to project not only to M1 but also to the ventral
and dorsal subdivisions of premotor cortex and the supplementary motor
area. These findings suggest that an integrated map of the body is represented
within the motor domain of the dentate and its connections.
Doya (1999, 2000)’s framework applies machine learning concepts to
different brain areas’ computational contributions (see Fig. 7.1). In this
framework, the cerebellum is specialized for supervised learning as its
Figure 7.1 Regions of the brain with substantial contributions to motor skill and the
computations believed to be central to each region. Reproduced with permission from
Doya (2000).
canonical computation. The role of the cerebellum for motor skill is to

maintain an accurate internal model of the motor system. It does this by con-
tinually updating the current state of the motor system by comparing the
predicted sensory feedback from a motor command to the actual feedback.
The result of this comparison is an error signal, making this computation a
form of “supervised” learning.
3.1.2 Cerebellar findings in ASD

A comprehensive review of the cerebellum in terms of anatomy, physiology,
and contribution to behavior in ASD was recently published (Fatemi et al.,
2012) and can also be found in Chapter 1 of this volume by Becker and
Stoodley. Here, we will focus on atypical aspects of the cerebellum that
are likely to bear on motor skill learning and performance.
The most consistent findings are in the cerebellar hemispheres and ver-
mis. Autopsy studies have found reduced numbers of Purkinje cells in the
cerebellar vermis and hemispheres, with cerebellar anatomical abnormality
found in 21–25 of all 29 (72–86%) cases in which the cerebellum was exam-
ined by six independent lab groups (Bailey et al., 1998; Bauman & Kemper,
1994; Fehlow, Bernstein, Tennstedt, & Walther, 1993; Kemper & Bauman,
1998; Ritvo et al., 1986; Williams, Hauser, Purpura, DeLong, & Swisher,
1980; and reviewed in Bauman & Kemper, 2005). Purkinje cell loss in
autism is patchy, and the amount and distribution of loss across the cerebellar
hemispheres and vermis differ from individual to individual. Neural ectopias
in the inferior cerebellar peduncle and malformation of the inferior olives, a
crucial afferent structure of the cerebellum, have been found (Bailey et al.,
1998; Kemper & Bauman, 1998; Rodier, Ingram, Tisdale, Nelson, &
Romano, 1996).
Structural imaging studies of the cerebellum have repeatedly revealed
hypoplasia or underdevelopment of the cerebellar vermis. The first quanti-
tative MRI studies identified abnormally reduced size of cerebellar hemi-
spheres (Gaffney, Tsai, Kuperman, & Minchin, 1987; Murakami,
Courchesne, Press, Yeung-Courchesne, & Hesselink, 1989) and subregions
within the vermis in autistic children and adults (Courchesne, Hesselink,
Jernigan, & Yeung-Courchesne, 1987; Courchesne, Yeung-Courchesne,
Press, Hesselink, & Jernigan, 1988). Twelve additional studies with a total
of several hundred subjects from seven independent labs reported signifi-
cantly reduced size in one or another subregion of the vermis (Carper &
Courchesne, 2000; Ciesielski & Akshoomoff, 1990; Ciesielski, Harris,
Hart, & Pabst, 1997; Ciesielski & Knight, 1994; Courchesne et al., 2001,
1994; Hashimoto et al., 1995; Kates et al., 1998; Kaufmann et al., 2003;
Levitt et al., 1999; Saitoh, Courchesne, Egaas, Lincoln, & Schreibman,
1995; Zilbovicius et al., 1995) or hemispheres (Courchesne et al., 2001)
or in overall cerebellar gray matter (McAlonan et al., 2002). In some few
cases, cerebellar size reduction is so substantial as to be detected by visual
inspection (Miles & Hillman, 2000). Some studies have associated anatom-
ical abnormality with severity of symptoms (Ecker et al., 2012; O’Halloran,
Kinsella, & Storey, 2012). Functional imaging studies of the cerebellum
reveal an unfortunate mix of results—increases, decreases, and unchanged
activation in children with ASD. These discrepancies could emerge from
methodological differences, age-related differences between typical and
neurodevelopmentally delayed populations, and artifact-creating movement
during scanning (Brown & Jernigan, 2012). Looking at motor production
during a finger-tapping task that was designed to be cognitively simple,
thereby isolating movement, has revealed an increase in activity in the ipsi-
lateral anterior cerebellum along with cerebellar regions not typically rec-
ruited for finger tapping (Allen, Muller, & Courchesne, 2004). However,
during another finger-tapping task, Mostofsky and colleagues showed
decreased ipsilateral anterior cerebellar activity and increased supplementary
motor cortical activity in children with high-functioning autism (Mostofsky
et al., 2009).
3.1.3 Cortico-basal ganglia loops

The complexity of basal ganglia circuitry has impeded the progress of map-
ping information from anatomical descriptions to functional descriptions in
behaving animals, despite receiving decades of intense study. The striatum
(caudate and putamen) is the gateway to the basal ganglia, and it collects
information from all areas of the cortex and portions of the thalamus and
the amygdala. Striatal medium spiny neurons (MSNs) have two projection
patterns. The “direct” pathway is from the striatum to the internal segment
of the globus pallidus (GPi) and substantia nigra pars reticulata (SNr). In the
classic model of basal ganglia function, the direct pathway facilitates move-
ment by releasing tonic inhibition of the thalamus. The “indirect” pathway
is modulatory and has MSNs projecting to the external segment of the
globus pallidus (GPe) and the subthalamus, which in turn project back to
the GPi. In the classic model, the indirect pathway is thought to inhibit
movement. MSNs of both pathways receive dopaminergic modulatory
input from the substantia nigra pars compacta (SNc); however, the receptors
on direct and indirect pathway MSNs are different and are believed to be
primary to the different actions of the two pathways (Graybiel, Aosaki,

Flaherty, & Kimura, 1994).
The role of basal ganglia in its connections with the cortex appears to be
in selecting the correct action from many based on expected value (Balleine,
Delgado, & Hikosaka, 2007; Graybiel, 1995a, 1995b) through reinforce-
ment learning (see Fig. 7.1). Past experience with reward and costs associated
with different behaviors are maintained in the basal ganglia with dopamine
neurons contributing to a prediction of expected reward. In this view, the
role of the basal ganglia is to select the most appropriate (most rewarding)
movement for the current state and suppress all others for individual and
sequential movements. Current studies of basal ganglia contributions to
movement are more nuanced and focused on the early learning of coordi-
nating movement sequences and mapping action policies to changing move-
ment goals (Kravitz & Kreitzer, 2012; Shmuelof & Krakauer, 2011). Yet
another view suggests that the direct and indirect pathways, instead of facil-
itating and inhibiting movements, are better thought of as comparing the
benefits of a certain action plan (direct pathway) with the costs (indirect
pathway) (Hwang, 2013).
Reinforcement learning (see Fig. 7.1) is based on a calculation of error
between expectation and actual reward. Reward in this setting is an odd
concept because a successful movement can be considered to be rewarding
in and of itself (Shadmehr, Orban de Xivry, Xu-Wilson, & Shih, 2010).
However, recent eye movement data reveal that movements to more valued
targets tend to be faster (Shadmehr, 2010; Shadmehr et al., 2010). These data
offer a perspective that considers not only the rewarding aspects of each
movement but also the costs associated with each movement—in this case,
the costs associated with delaying reward. Although most examinations of
reinforcement learning concern a simple two-alternative forced-choice par-
adigm, reinforcement learning appears to be successful in guiding optimal
choice in a more complex environment, for example, in learning an “opti-
mal” habit (Desrochers, Jin, Goodman, & Graybiel, 2010; Sejnowski, 2010)
and in finding a hidden target with one’s eye movements (Chukoskie,
Snider, Mozer, Krauzlis, & Sejnowski, 2013).
Redgrave and colleagues have suggested a framework in which the basal
ganglia are considered in terms of specialization for “goal-directed” versus
“habitual” movement (Redgrave et al., 2010), with the dorsomedial basal
ganglia being goal-directed and the dorsolateral being habit-directed.
Goal-directed movements are flexible but slow to learn and require consid-
erable computation, whereas habitual movements are fast but inflexible.
Which system should be engaged for a given scenario? Daw, Niv, and Dayan
(2005) proposed a method for choosing which action system is the best by
minimizing the uncertainty of predictions produced by the goal or habit
systems.
3.1.4 Basal ganglia findings in ASD

The basal ganglia are hypothesized to be crucial for skill-based learning
(Hikosaka et al., 2002). Not surprisingly, given the motor deficits observed
in ASD, several researchers have specifically examined the basal ganglia for
differences that might explain the motor and other behaviors observed in
ASD. Vilensky and colleagues measured several aspects of gait in children
with autism (Vilensky et al., 1981) and noted that many atypical aspects
of gait were reminiscent of gait in Parkinson’s disease. Hence, these authors
and others suggested looking at the basal ganglia as a possible source of motor
dysfunction in autism. Several anatomical imaging studies have found that
the basal ganglia size relative to the rest of the brain or basal ganglia shape
is different in individuals with ASD (Ecker et al., 2012; Hollander et al.,
2005; Langen, Durston, Staal, Palmen, & van Engeland, 2007; Sears
et al., 1999). In addition, the shape of different right posterior putamen
and bilateral anterior putamen of the basal ganglia predicts aspects of motor
dysfunction in boys with ASD (Qiu, Adler, Crocetti, Miller, & Mostofsky,
2010). The right posterior putamen, which forms a circuit with right motor
cortex, is believed to be involved with sensory guidance for goal-directed
movements, while bilateral anterior putamen connects with bilateral
premotor regions and is involved with the selection and sequencing of
skilled movements.
Beyond the relative size and shape of the basal ganglia, the connections to
and from the basal ganglia may be atypical, leading to altered communica-
tion between this motor and reward region and various regions of the cor-
tex. The results have been heterogeneous, likely due to differing methods
and also different pathways examined. Atypical reward processing has been
studied using functional imaging, comparing responses due to social versus
monetary rewards (Scott-Van Zeeland, Dapretto, Ghahremani, Poldrack, &
Bookheimer, 2010). These authors found reduced ventral striatal responses
to both social and monetary rewards in children with ASD as compared to
typically developing children. In addition, ventral striatal activity was asso-
ciated with poorer social functioning.
Di Martino and colleagues examined resting-state functional connectiv-
ity in a large population of children with ASD compared with both
typically developing children and also typical adults (Di Martino et al.,
2011) and consistently found atypically increased resting-state connectivity
in children with ASD. Interestingly, a study of connectivity in children,
who had ASD, ADHD, or both, found that the children diagnosed with
both had dysfunctional striatal circuitry, but not the children diagnosed
with ASD alone (Di Martino et al., 2013). This result suggests that comor-
bid symptoms are likely contributing to the heterogeneity of responses
observed in ASD. Fractional anisotropy (FA) of white matter tracts con-
necting the putamen with the frontal cortex was lower in adults with
autism (Langen et al., 2012). Performance on a go/no-go task was corre-
lated with FA in this white matter tract, suggesting that the inhibitory con-
trol needed for a go/no-go task is at least partially mediated by this tract.
A recent report showed dramatically decreased task-based connectivity
from reward-related regions of the basal ganglia to the posterior superior
temporal sulcus, a region believed to be involved in speech sound percep-
tion (Abrams et al., 2013).
Both basal ganglia volume and connectivity measures have been com-
pared with motor performance, again with mixed findings. Hardan,
Kilpatrick, Keshavan, and Minshew (2003) examined motor performance
with the grooved pegboard task, grip strength, and finger tapping. The
authors aimed to compare motor deficits observed in ASD to basal ganglia
volume estimates, but found no volume differences between the children
with ASD and typically developing children. Takarae and colleagues
showed increased bilateral activation of frontostriatal circuitry during a visu-
ally guided saccade task (Takarae, Minshew, Luna, & Sweeney, 2007).
Mostofsky and colleagues (Qiu et al., 2010) reported that the shape of the
basal ganglia is predictive of motor dysfunction using the PANESS assess-
ment battery and also social and communication skills. A correlation
between repetitive behaviors and the volume of the right caudate and total
putamen was reported (Dichter, 2012; Estes et al., 2011; Hollander
et al., 2005).
3.1.5 The cerebellum and basal ganglia are reciprocally connected

The cerebellum and basal ganglia have multiple loops that appear to be sep-
arated for motor and associative functions. These different subcortical loops
specialize in different types of computation for the purpose of learning, and
both of these subcortical systems have been reported to be atypical in both
anatomical and functional studies. Until recently, it was believed that these
two important subcortical systems interacted only via cortical areas through
which they both looped. However, we now know that the basal ganglia and
the cerebellum are reciprocally connected through disynaptic subcortical
connections (Bostan et al., 2013). These newly identified pathways recipro-
cally connect motor and associative regions of the cerebellum and basal
ganglia. Importantly, connections between the basal ganglia and cerebellum
bring “reinforcement learning” machinery together with “supervised learn-
ing” machinery.
What benefits would such a connection bring? There is not a precise
answer to that question, but optimal control theory offers a useful perspec-
tive. Todorov and Jordan have argued that we make movements to reach a
more rewarding state (Todorov & Jordan, 2002). Optimal control theory
describes a formal way to link motor costs, expected rewards, noise from
sensory feedback, and internal models of a movement. In this framework,
the basal ganglia and cerebellum are both engaged in feedback loops to opti-
mize motor control. The basal ganglia calculate expected costs of motor
commands and expected rewards of sensory feedback, whereas the cerebel-
lum, through internal models, predicts the visual and proprioceptive feed-
back expected as a consequence of a particular motor command. Through
feedback, both of these areas contribute to the refinement of future motor
commands, which would be essential in learning a motor skill and especially
a sequence of motor skills.
3.2. How do autism motor skill deficits fit in this framework?

Using the breadth and depth of the literature on motor control in typical
individuals and macaque monkeys, we can begin to evaluate whether
motor skill differences observed in individuals with ASD are deficits at
some level of motor planning or execution or instead a compensation made
to accommodate the demands of an altered nervous system state
(Shadmehr & Krakauer, 2008). For example, patients with acquired cere-
bellar damage may reach slowly as a learned response to an inability to pre-
dict sensory consequences of movements, and this inability is magnified in
an attempt to control fast movements. For a neurodevelopmental disorder
such as ASD, the problem is likely even more complex, because the system
adapts to new abilities that come on line during development as would be
expected, but it is also compensating for deficits or inabilities that arise in
the system as new movement behaviors are learned. Here, we consider the
computations of the cerebellum and basal ganglia in terms of the motor skill
deficits observed in ASD.
3.2.1 Is there a problem with the “supervised learning” circuitry

of the cerebellum? (Fig. 7.1)
Certainly, this could be the case as the major output neurons—the Purkinje
cells—are the leading cited anatomical finding in postmortem histological
analyses, a finding that has been echoed in animal models of autism
symptomology including maternal immune activation (Shi et al., 2009)
and Tsc1 TSC1 (Tsai et al., 2012) and Gabrb3 knockout mice (DeLorey,
Sahbaie, Hashemi, Homanics, & Clark, 2008).
The cerebellum has been generalized as the site for prediction and prep-
aration for coordinating motor action, but not only for movement. Cer-
tainly, many of the motor results observed in autism can generally be
categorized as a deficit in preparation or prediction for a movement plan.
Note that we would not expect a complete failure in preparation or predic-
tion because other areas of the motor system compensate for congenital or
acquired deficits of the cerebellum. Perhaps, a deficit in the circuitry, which
calculates and makes the motor error comparison, could produce this pattern
of deficits. Variability in either the target representation or the copy of the
motor command (corollary discharge) would result in a noisy error signal
(Kording & Wolpert, 2006).
Pursuit eye movement experiments have indicated that a “closed-loop”
or “feedback-involved” velocity deficit suggests either cerebellar or long-
range cortical pathology in individuals with ASD. The middle temporal
(area MT) and middle superior temporal (area MST) cortical areas contrib-
ute to the pursuit process with area MST combining the extraretinal infor-
mation about eye movement with pure sensory information about motion
(Chukoskie & Movshon, 2009). The role of the cerebellum in delivering
precise feedback and controlling movement variability also makes it relevant
to the saccade timing and metrical differences observed in individuals with
ASD (Luna et al., 2007; Nowinski, Minshew, Luna, Takarae, & Sweeney,
2005; Takarae et al., 2004). In fact, fMRI activation of the oculomotor ver-
mis was reduced in individuals with ASD compared to typically developing
individuals during a saccade task (Takarae et al., 2007).
Adaptation is perhaps the classic cerebellar task. The internal model of
the relevant effector system (arm, leg, eye, etc.) must be altered to accom-
modate the ongoing changes in that movement effector system throughout
the life of the organism. Adaptation experiments were designed to under-
stand the motor learning that must accompany an ever-changing motor sys-
tem. If the cerebellum is affected as we expect in ASD, then we would
anticipate deficits in adaptation. In a study using both a ball-throwing task
with prism goggles and a novel-reaching task with forces imposed via a
robotic arm (Gidley Larson, Bastian, Donchin, Shadmehr, & Mostofsky,
2008), children with ASD learned quickly and exhibited typical aftereffects,
suggesting that a failure to update the internal model is not the source of
motor skill deficits in autism. However, recent data suggest that this is indeed
an area of concern in individuals with ASD, at least where eye movements
are concerned. In a recent saccade adaptation experiments in individuals
with ASD (Mosconi et al., 2013), approximately 30% of the subjects with
ASD did not adapt at all (compared with 6% of control subjects). Those indi-
viduals with ASD who did adapt did so more slowly and also showed
increased trial-to-trial variability in saccade amplitudes. Another recent sac-
cade adaptation experiment revealed similar results but notably also exam-
ined adaptation of children with Asperger’s syndrome ( Johnson, Rinehart,
White, Millist, & Fielding, 2013). The authors found weaker adaptation in
children with autism and Asperger’s syndrome compared to typically devel-
oped children. These results indicate deficits in the learning mechanisms of
the oculomotor vermis; however, the increased amplitude variability could
result in “noisy” information feeding into the calculated error signal
(Havermann & Lappe, 2010).
3.2.2 Is the basal ganglia “reinforcement learning circuitry” different

in ASD?
If one role of the basal ganglia is to help select the best action for the situation
in a timely manner, then the slow movements and difficulty with creating
movement sequences suggest that we should look further at the basal ganglia.
Basic motor deficits, such as in initiation and accuracy, can lead to poor or
absent reinforcement. In addition, what is rewarding in autism is quite likely
to be different than in typical development, and this may factor into how
individuals with ASD move. Targets that are valued differently by the actor
elicit different movements, in terms of latencies, movement speed, and accu-
racy. Motivation also impacts response vigor purportedly through tonic
dopamine levels (Niv, Daw, Joel, & Dayan, 2007). Although we do not
yet have the data in autism, the framework for comparison exists. Specifi-
cally, with respect to saccades, a thorough analysis of the main
sequence—the relationship between movement amplitude and velocity—
appears to be modified by one’s willingness to wait for the target reward
(Shadmehr et al., 2010). For example, the inclination to discount reward
over time is increased for young children—they would prefer to have
one marshmallow now versus two in a few minutes. The higher temporal
discount rate for children nicely matches their faster saccades for any given
amplitude. Similar data exist for individuals with schizophrenia (who also
have a higher temporal discount rate (Shadmehr et al., 2010). However,
we still lack data that span a range of directions and amplitudes in a matched
sample of individuals with ASD and typically developed individuals.
Some regions of the basal ganglia are more specialized for “goals” versus
“habits” (Redgrave et al., 2010). By examining the activity of particular
regions of the basal ganglia with respect to each other, one might learn
whether individuals with ASD have a biased use of basal ganglia circuitry,
for example, they may be more goal-directed in their actions versus habitual.
Referring back to Daw and colleagues’ perspective on using uncertainty to
choose which action system to use (Daw et al., 2005), it is possible that goal-
directed or habitual actions might be noisier in individuals with ASD, bias-
ing the choice toward the more reliable system.
3.2.3 Functional connectivity, including in cortex, likely impacts motor

skill in ASD
Modern perspectives on autism (Abrahams & Geschwind, 2010;
Geschwind & Levitt, 2007) along with both diffusion tensor imaging
(Ameis et al., 2011; Shukla, Keehn, & Muller, 2010; Wolff et al., 2012)
and postmortem anatomy (Zikopoulos & Barbas, 2010) data hold that
intercortical connectivity is atypical in ASD. This result has myriad impli-
cations for motor planning, not the least of which is the feedback of sensory
information to inform planning of future motor commands. We know from
many reports that sensory perception is atypical in many individuals with
ASD, though this too suffers from a lack of quantification in most studies.
Whether this also means that the neural representation of a sensory event
in terms of location and timing is atypical remains an open question, but
if it does, it would also impact the quality of motor skill.
4. CAN WE INTERVENE?
What happens in the brain during motor skill learning? This question
can be asked at many levels, including synaptic and subsynaptic, functional
motor maps and activity, and at a range of temporal scales. Figure 7.2 rep-
resents a summary of motor skill training effects modifying the efficacy of
synapses in the cerebellum and basal ganglia based on animal research
findings.
A
Climbing
Parallel fibers
fiber
Purkinje cells
B
Pyramidal cells
Cortex
Striatum
MSNs
Interneuron
Figure 7.2 (A) Summary of acrobatic motor skill training-induced plasticity in the cerebel-
lum. Yellow stars indicate putative sites for training-induced synaptic strengthening. Par-
allel fiber (red) to Purkinje cell (blue) synapses were significantly increased, while climbing
fiber (yellow) synapses showed a trend toward increasing. (B) Stars indicate putative sites of
training-induced plasticity in the basal ganglia. Medium spiny neurons of the direct (green)
and indirect (blue) pathways are depicted along with descending input from cortical pyra-
midal cells (black, purple) and striatal interneurons (yellow). Adapted with permission from
Kreitzer and Malenka (2008).
Two models of motor skill learning propose interactions between two

cortical–subcortical circuits, but these models differ in the specialty of those
two loops (for a review, see Dayan & Cohen, 2011). Hikosaka et al. (2002)
described a framework for interpreting which areas are involved in sequen-
tial motor skill learning. The authors propose two parallel loops specialized
for learning spatial and motor features of sequences. In this model, the two
loops are connected through premotor and supplementary cortical areas, and
the “spatial coordinate” loop involves associative frontoparietal cortices
connecting with associative regions of the striatum and cerebellum. The
“motor coordinate” loop connects primary and sensorimotor cortices with
the motor regions of the striatum and cerebellum. Functionally, the spatial
coordinate loop is faster but requires more attention and executive function
resources. The motor coordinate loop can be considered more habitual in
that learning is slow and implicit but once learned, attentional load is
low. This framework and that of Redgrave may create useful links by relat-
ing goals and spatial coordinate loops on one hand and habits and motor
coordinate loops on the other (Redgrave et al., 2010). Doyon and colleagues
(Doyon, Penhune, & Ungerleider, 2003) also proposed a two-loop model
with interactions between them essential for motor skill learning. However,
in this model, fast learning demanded both loops through the cortex, stria-
tum, and thalamus as well as cortex, cerebellum, and thalamus. More recent
data demonstrating disynaptic connections between the cerebellum and
basal ganglia (Bostan et al., 2013) could provide further insight into the
motor learning-related activity of these loops.
4.1. Motor skill training in rodents

Motor training works by reorganizing brain connectivity. Animal research
has revealed several neural mechanisms that underlie behavioral improve-
ments that result from motor training. Studies of forelimb-reaching training
in rats, which takes place over only 10–14 days, create an expansion of the
forelimb region in primary motor cortex (Greenough, Larson, & Withers,
1985), and it is known how the motor map plasticity induced by this training
is regulated (Conner, Culberson, Packowski, Chiba, & Tuszynski, 2003). At
a finer level of detail, researchers have studied the changes in dendritic spine
movement and contact as training progresses (Fu, Yu, Lu, & Zuo, 2012).
Greenough and colleagues (Black, Isaacs, Anderson, Alcantara, &
Greenough, 1990) have observed synaptogenesis in the cerebellum, at the
level of rat Purkinje cells (see Fig. 7.2A) after “acrobatic” training, involving
whole-body balance coordination to navigate obstacles. Synaptogenesis was

observed in contrast to increased cerebellar vascularization in the para-
median lobule when the rats ran with no special coordination or balance
corrections for the same amount of time as the acrobatic training. A later
study showed that the increase in molecular layer volume after acrobatic
training was due to a change in the parallel fiber (PF) synapses onto Purkinje
cells (Kleim et al., 1998). Climbing fibers (CFs) have a large physiological
effect on Purkinje cell response in experiments comparing CF versus PF
stimulation. In the acrobatic rat study, CF-Purkinje cell synapses showed
a trend toward an increase in number but did not increase significantly in
the Kleim et al.’s study. The cerebellar synaptogenesis effects were observed
in typical young adult rats; however, the training effects are also observed in
animals, which experienced early life brain damage. Both the behavioral and
cellular changes were observed in rats with a cerebellar deficit resulting from
perinatal alcohol exposure (Klintsova et al., 1998, 2002). Recent studies
have also detailed the emergence of PF multisynapse boutons contacting
Purkinje cell spines as a result of motor training (Lee et al., 2013).
Naviaux et al. (2013) recently showed that antipurinergic therapy in
young maternal immune activation mice appeared to prevent the dramatic
Purkinje cell loss typically observed in that animal model. The idea of inter-
vention to prevent the development of further dysfunction suggests consid-
eration of optimal time windows for certain motor interventions. However,
it is also worth noting that balance skill training in elderly people is effective
at preventing falls (Clemson et al., 2012; Granacher, Gollhofer, Hortobagyi,
Kressig, & Muehlbauer, 2013; Sherrington, Tiedemann, Fairhall, Close, &
Lord, 2011), demonstrating clearly that motor plasticity continues into
later life.
Our understanding of how motor learning engages plasticity in the basal
ganglia has expanded substantially in the past decade, but many questions still
remain. Disruptions of long-term potentiation, by blocking NMDA recep-
tors from cortical projections onto MSNs of the dorsomedial striatum, also
impair goal-directed learning (Yin, Knowlton, & Balleine, 2005). Blocking
dopamine receptors in the direct pathway (D1 receptors) in the dorsomedial
striatum decreases reward-dependent learning in a saccadic eye movement
task (Nakamura & Hikosaka, 2006). Rodent models of Parkinson’s disease
have also suggested that long-term depression at indirect pathway synapses is
essential for normal movement (Kreitzer & Malenka, 2007). Kreitzer and
Malenka (2008) reviewed the literature and indicated sites of likely plasticity
given our understanding of the connectivity between cortex and striatum
and between direct and indirect pathway MSNs (see Fig. 7.2B). These phys-
iological measures of synaptic plasticity echo the structural changes reported
in the cerebellum and motor cortex during acrobatic training. This is still a
rather active area of research in which the recent development of
optogenetic techniques applied to the basal ganglia (Kravitz et al., 2010)
is especially promising for unifying our understanding of the changes motor
learning creates across different brain regions.
4.2. Motor training for children with ASD?

The insidious aspect of motor skill failure is that it feeds upon itself. Those
with less motor skill are less likely to move and therefore less likely to
develop improved motor skill. In a culture saturated with the performance
of elite athletes who train year-round to maintain their status as such, it seems
hardly necessary to make the point that training improves motor skill. How-
ever, one might rightly question whether motor training will be similarly
successful in individuals with ASD and whether training can alter the specific
differences observed in, for example, a proprioceptive bias in an internal
model for reaching behavior (Haswell et al., 2009).
To answer this question, we consider two points. First, one of the widely
used and successful early interventions for ASD is known as DIR/Floortime
(Greenspan et al., 2008). This, in addition to sensorimotor integration ther-
apy, has been used by occupational therapists for children with ASD (Baranek,
2002). One of the aims of these interventions is to help the child plan appro-
priate movements that assist his or her engagement with the surrounding envi-
ronment. Second, although we found no published studies of balance training
for individuals with ASD, balance training, using the WBB and games,
has been successful for individuals with Down’s syndrome (Berg, Becker,
Martian, Primrose, & Wingen, 2012; Wuang, Chiang, Su, & Wang, 2011)
and largely successful for individuals with cerebral palsy (Deutsch, Borbely,
Filler, Huhn, & Guarrera-Bowlby, 2008; Shih, Shih, & Chu, 2010).
Ramstrand and colleagues (Ramstrand & Lygnegard, 2012) failed to find bal-
ance improvements in children with cerebral palsy after WBB training,
while Jelsma and colleagues ( Jelsma, Pronk, Ferguson, & Jelsma-Smit,
2013) found improvements in balance but not in other markers of fitness such
as speed of running, agility, or time to go up and down stairs in this population.
A recent study of children with degenerative ataxia found significant improve-
ment in dynamic balance following training with Kinect Xbox games
(Ilg et al., 2012).
Training motor skills may have additional benefits beyond those specific
to motor function. Recent findings in typically developing infants show that
early infant milestones such as learning to reach are foundational for later
social skill components such as social gaze preference (Libertus &
Needham, 2011). Coordination and speed of movement correlate positively
with cognitive measures in typical preschool aged boys and girls (Planinsec,
2002). Studies of DCD, in which there is substantial overlap with ASD
(Kopp, Beckung, & Gillberg, 2010; Piek & Dyck, 2004), show poorer social
skills in individuals with greater motor deficits. A recent paper also reveals
that poorer balance skills are associated with increased repetitive behaviors
(Radonovich, Fournier, & Hass, 2013). These data suggest that training-
induced improvements in a foundational motor skill, such as balance, might
have positive effects on other autism symptoms.
4.3. Motor training for older adults with ASD?

ASD is a relatively “modern” disorder; the children first described by Kanner
and Asperger would be turning 80 this year. There is as yet little published
research focused specifically on older adults with ASD; other than the data
suggesting a higher mortality rate (Bilder et al., 2013; Gillberg, Billstedt,
Sundh, & Gillberg, 2010; Shavelle, Strauss, & Pickett, 2001), recent papers
have primarily highlighted the lack of knowledge in this area (Happe &
Charlton, 2012; Janicki, Henderson, & Rubin, 2008; Mukaetova-
Ladinska, Perry, Baron, & Povey, 2012; Piven & Rabins, 2011). There
may be abnormal age-related structural changes in adults with ASD
(Murphy, Beecham, Craig, & Ecker, 2011), but even if the developmental
trajectory in ASD does not differ from that of typical older adults, ASD-
related motor deficits should be of special concern. Balance skill and muscle
strength degrade in the elderly, leading to an increased risk of falls. The Cen-
ters for Disease Control and Prevention reports that falls are the leading cause
of injury among adults 65 and older and projects that the total direct and
indirect cost of fall injuries among the elderly is expected to reach $55.9 bil-
lion in 2020 (Older Adult Falls Data & Hallgato, Gyori-Dani, Pekar,
Janacsek, & Nemeth, 2013). Motor systems that are already compromised
are likely to be more susceptible to age-related degradation, and given
the increasing rates of autism, this could be a major public health concern.
Interventions targeting balance and core and lower-limb strength in typical
elderly have shown to be effective at reducing the risk of falls (Clemson et al.,
2012; Granacher et al., 2013; Sherrington et al., 2011). As the ASD
population ages, with intrinsically less balance skill, we should expect an

increasing incidence of falls unless interventions specifically target a change
in motor competence.
5. SUMMARY
This review of data on motor skills with anatomical and connectivity
differences in individuals with ASD places us in a position to consider what
questions, if answered, would take us to the next step in understanding the
motor skill in ASD. The questions in Box 7.1 are the proverbial tip of the
iceberg, but attempting to answer them will take us to the next stage of our
understanding.
Despite the increased interest in motor skills in autism, most of the
reports described earlier contain primarily descriptive data. If we are to
use motor skill differences to understand more about the nervous system
in autism, we need more quantitative and computational characterizations
of the motor control differences in individuals with ASD. In this review,
we have examined the data from the perspective of subcortical motor
centers—the cerebellum and basal ganglia and their cortical loops—as a
starting point for understanding the acquisition and performance of skilled
movements in ASD. We have also pointed to areas of movement research
in typically developing individuals that might be beneficial to consider for
understanding motor skill in ASD. By thinking about the types of compu-
tational roles performed by the different motor regions, we can design
future motor skill experiments that probe these roles explicitly and,
through greater understanding of motor skill deficits, design effective
interventions.
BOX 7.1 Open questions about motor skill in individuals with ASD
What does the developmental trajectory of motor skill look like in ASD?
Where are the delays?
Where are the deficits?
How reliable is the sensory and corollary discharge feedback in
individuals ASD?
Is there a bias for goal-directed or habitual movements in individuals
with ASD?
What differences exist in terms of motor costs and sensory rewards in ASD
compared with typical development?
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Motor Skill in Autism Spectrum Disorders: A Subcortical View

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CHAPTER SEVEN

Motor Skill in Autism Spectrum

International Review of Neurobiology, Volume 113 # 2013 Elsevier Inc. 207

1. WHY STUDY MOTOR SKILL IN AUTISM?

1.1. Motor skill as foundational in development

1.2. Early signs are motor

1.3. Correlation with social and communication skill

remains an understudied domain in ASD and we are only beginning to

2. OVERVIEW OF MOTOR SKILL DEFICITS

2.1. Gross motor skills

performing anticipatory postural adjustments, such as one would make to grab

reach-to-grasp movement that varied with intellectual ability in a sample of

2.2. Fine motor skills

Illegible handwriting was specifically noted by Hans Asperger in his initial

2.4. Eye movements

3. MAPPING AUTISM MOTOR SKILL FINDINGS

3.1. Cortico–subcortical loops for motor control

3.1.1 Corticocerebellar loops

canonical computation. The role of the cerebellum for motor skill is to

3.1.2 Cerebellar findings in ASD

3.1.3 Cortico-basal ganglia loops

primary to the different actions of the two pathways (Graybiel, Aosaki,

3.1.4 Basal ganglia findings in ASD

3.1.5 The cerebellum and basal ganglia are reciprocally connected

3.2. How do autism motor skill deficits fit in this framework?

3.2.1 Is there a problem with the “supervised learning” circuitry

3.2.2 Is the basal ganglia “reinforcement learning circuitry” different

3.2.3 Functional connectivity, including in cortex, likely impacts motor

Two models of motor skill learning propose interactions between two

4.1. Motor skill training in rodents

whole-body balance coordination to navigate obstacles. Synaptogenesis was

4.2. Motor training for children with ASD?

4.3. Motor training for older adults with ASD?

population ages, with intrinsically less balance skill, we should expect an

Royal Society of London Series B, Biological Sciences, 358(1430), 393–403. http://dx.doi.

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