Autism Spectrum Disorder (ASD) is traditionally characterized by deficits in social interaction, communication, and restricted repetitive and stereotyped patterns of behaviors, interests, and activities (American Psychiatric Association, 2000). Although there will be changes to the diagnostic criteria with the DSM-V, the proposed criteria maintain focus on social/communicative symptoms and restricted/repetitive behaviors (Wing et al., 2011; Nishawala, 2012). This focus is maintained despite research demonstrating an extended profile of ASD that includes movement impairments (Staples and Reid, 2010; MacNeil and Mostofsky, 2012; Whyatt and Craig, 2012). Movement research has vast implications for treatment and therapy for individuals with autism, as the coordination and regulation of sensory and movement information is required for social interaction, speech communication, and participation in the environment (Donnellan et al., 2012). Since movement is a new area of consideration in ASD, there are few research studies focused on accommodations or treatments to improve movement in children with ASD. One accommodation that has not yet been explored is the use of rhythmic cueing to improve sensorimotor functioning in ASD.

Recent comprehensive research reviews have established that auditory rhythmic cueing is an effective tool for gross motor rehabilitation in populations including stroke (Bradt et al., 2010) and Parkinson's disease (de Dreu et al., 2012). Success observed with these populations has been attributed to processing of rhythm in the brain, motor synchronization to an auditory stimulus, and the intact motor synchronization ability of persons with neurological disease and disorder. Furthermore, rhythmic cueing is proposed to activate motor neurons via reticulospinal pathways, effectively priming the motor system (Rossignol and Melvill Jones, 1976; Thaut, 2005). Based on this rehabilitation research, we propose that rhythm may also be used in the treatment of movement differences in individuals with ASD. The purpose of this paper is to illustrate the potential impact of rhythmic cueing for sensorimotor regulation in persons with ASD. To this effect, we review research on rhythm in motor rehabilitation, draw parallels to motor dysfunction in autism resulting primarily from differences in the cerebellum, and propose a rationale for how rhythmic input can improve motor functioning, based on initial research indicating that rhythmic synchronization is intact despite cerebellar deficits. Furthermore, the potential benefits of rhythm for social/communicative behaviors will be explored.

Over the past two decades, researchers have begun to understand the neurological basis of music in the brain. Researchers have demonstrated that music processing and production are distributed throughout the cortex, subcortex, and cerebellum (Peretz and Zatorre, 2005). Areas engaged with music perception and production are not unique to music; rather, they overlap with non-musical networks (Thaut, 2005; Patel, 2011). Furthermore, the distributed nature of music in the brain allows preservation of musical functions despite the loss of a related non-musical function. For example, in persons with non-fluent aphasia, the ability to sing is unimpaired despite loss of speech production (Özdemir et al., 2006; Schlaug et al., 2009b). Research findings in music neuroscience have led to the development of neurologic music therapy techniques that drive cortical plasticity for rehabilitative gain.

Elements of music have been used effectively in therapy in collaboration as well as in isolation for various therapeutic needs. These elements include melody, harmony, tempo, dynamics, timbre, form, and rhythm. The organizing factor in all music is rhythm; therefore, rhythm serves as a timekeeper in the therapeutic application of music for motor rehabilitation goals and is foundational to auditory-motor synchronization. Auditory rhythmic cueing refers to an auditory sound stimulus with a fixed inter stimulus interval (such as the output from a metronome). As rhythmic cueing is well-documented to facilitate motor improvements in persons with neurological impairments, this paper will hypothesize the role of auditory rhythmic cueing in motor improvement in autism.

Bengtsson et al. (2009) demonstrated that auditory rhythm activates motor areas of the brain including the pre-motor cortex, supplementary motor areas, pre-supplementary motor area, and the lateral cerebellum. Rhythm not only activates motor areas of the brain, there is evidence of rapid motor synchronization to an external rhythmic cue in persons with and without neurological disability (Thaut et al., 1999a). Initial evidence of auditory-motor synchronization led to investigation of the auditory-motor pathway, with suggested involvement of the reticulospinal connections (Rossignol and Melvill Jones, 1976), cerebellum, brainstem, and the basal ganglia (Thaut and Abiru, 2010). This unique relationship between rhythm and motor function has been studied extensively in the rehabilitation sciences, where auditory rhythmic cueing has been utilized as an effective treatment in motor rehabilitation for over a decade (Thaut, 2005). There are two primary factors that contribute to the success of auditory rhythm in rehabilitation (1) rhythmic synchronization and (2) evidence that rhythmic cueing used systematically can facilitate cortical plasticity.

Motor disturbances are not part of proposed DSM-V diagnostic criteria of autism; however, growing evidence indicates that neurological dysfunction may be associated with abnormal movements seen in individuals with autism. In a study of 67 children with ASD, Hilton et al. (2012) found that 83% of children with ASD presented motor scores at least one standard deviation below the general population, with greater impairments seen in children with more severe autism. This was compared to 6% of children from the same families without ASD showing a similar deficit. Other studies have estimated that between 80 and 90% of children with ASD demonstrate some degree of motor abnormality (Ghaziuddin and Butler, 1998; Dziuk et al., 2007; Ming et al., 2007; David et al., 2009). Although studies focused on incidence of motor abnormality are relatively recent, the earliest description of ASD included motor differences.

In Kanner's earliest paper describing autism (1943), he acknowledged a variety of motor differences in the individuals with autism he observed. He noticed that while all of the children demonstrated skilled fine muscle coordination, several of the children exhibited clumsiness in gait and gross motor performances. He observed individuals with autism failing to assume an anticipatory posture as well as passive positioning like “a sack of flour” (p. 243). In some cases, the individuals he studied lacked the ability to adjust their body to the person holding them. Kanner also noted that the children's verbal utterances and motor performances were monotonous and repetitive, “resulting in marked limitation in the variety of spontaneous activity” (p. 245). He proposed that if the slightest element of a given action was modified, altered, or removed, it was not considered the same or accepted as such by the child (Kanner, 1943).

Since these earliest reports, researchers documented motor impairments in ASD including clumsiness and poor coordination (Hallett et al., 1993; Teitelbaum et al., 1998; Vernazza-Martin et al., 2005), gait abnormalities (Hallett et al., 1993; Vernazza-Martin et al., 2005; Rinehart et al., 2006), impaired performance of skilled motor tasks (Dewey, 1995; Mostofsky et al., 2006; Dziuk et al., 2007), and motor planning deficits (Rinehart et al., 2001; Schmitz et al., 2003; Gidley Larson et al., 2008; Fabbri-Destro et al., 2009). Motor deficits could have vast implications for communicative and social functioning, as these skills rely on the organization of sensory and motor responses (Donnellan et al., 2012). Teitelbaum et al. (1998, 2002) indicated that motor differences were apparent in infancy, including differences in the development of infantile reflexes, which may be indicative of a neurological difference in early childhood. Although researchers have documented abnormalities in nearly every brain system in persons with ASD (Minshew, 1994; Ciaranello and Ciaranello, 1995; Courchesne and Allen, 1997), MRI, and autopsy studies have consistently reported that the cerebellum is a common site of neuroanatomic abnormality.

Differences observed in the cerebellum of persons with ASD have included hyperplasia or hypoplasia of cerebellar hemispheres (Murakami et al., 1989; Hardan et al., 2001; Pierce and Courchesne, 2001) and one or more regions of cerebellar vermis (Pierce and Courchesne, 2001; Schmidt, 2002; Allen and Courchesne, 2003), and differences in the presence of Purkinje neurons (Kemper and Bauman, 1998; Allen and Courchesne, 2003). Fatemi et al. (2012) recently reviewed literature on the cerebellum in ASD and found points of consensus including abnormal anatomy, abnormal neurotransmitter systems, deficits in cerebellar motor and cognition, and neuroinflammation. The authors of this consensus paper presented evidence of a clear difference in cerebellar anatomy and function; however, the exact implications of these differences and treatment options are not yet understood (Fatemi et al., 2012).

Allen and Courchesne (1998) suggested that, based on connectivity, the cerebellum must function in both a general and highly integrative manner. These researchers suggested that the cerebellum may be responsible for purposes within multiple domains inclusive of cognitive, sensory, affective, and motor functions (Allen and Courchesne, 2003). Due to this widespread connectivity, Schmahmann and Pandya (2008) proposed that the cerebellum is involved with automatizing and optimizing functions around a “homeostatic baseline”; indicating that the cerebellum coordinates cognitive and emotional functions in the same way that it regulates and controls motor activity. Just as the cerebellum predicts the neural systems needed for a particular motor action, researchers suggest that it also predicts neural systems needed for a motor operation and then prepares for the operation at hand (Akshoomoff et al., 1997; Courchesne and Allen, 1997; Allen and Courchesne, 1998).

If the fundamental role of the cerebellum were to predict the neural systems needed to plan, adjust, and execute movements, then cerebellar damage or disease would likely affect the optimal functioning of a given neural system (Allen et al., 2004). Furthermore, the cerebellum's role in planning and coordinating movement would result in a lack of coordination in a person with cerebellar damage (Holmes, 1939). Persons with cerebellar damage maintain the ability to move; however, the quality and efficiency of movements is altered (Robinson, 1995). Although other neural systems continue to perform, they will do so sub-optimally without the preparatory role of the cerebellum to aid in performance (Allen et al., 2004). It is clear that individuals with ASD have the ability to move; however, Allen et al. (2004) proposed that they lack coordination due to a preparatory deficit. This preparatory deficit may account for the overall intact gross motor system that manifests differences in coordination and motor planning.

The findings that rhythmic synchronization behavior is intact in patients with both atrophic and focal cerebellar lesions suggests the possibility that rhythm could be utilized in motor differences in ASD despite the presence of cerebellar abnormalities. One of the findings in the cerebellum in autism is abnormal development of vermal lobules VI and VII (Carper and Courchesne, 2000). These areas are known to process auditory information on a more arousal-oriented level and activation of lobule VI revealed a time sensitive response to modifications of the rhythmic tempo (Thaut et al., 2009). In rhythmic synchronization tasks, Stephan et al. (2002) showed different cerebellar circuit involvement in varying aspects of the presented tasks. Activation in vermal regions ipsilateral to the movement was consistent in novel and/or complex tasks and resulted in activation that was incrementally larger in these areas (Stephan et al., 2002; Molinari et al., 2007). Rhythmic auditory cues may therefore facilitate activations in these areas to elicit shared networks for motor performance, or if needed, may provide compensatory accommodations to activate other areas. Further research in this area is needed in order to assess the impact of rhythmic auditory-motor cues in therapy in this population.

One proposed function of the cerebellum as “comparator” is to adjust motor output related to planned actions (Penhune et al., 1998; Zatorre et al., 2007). The cerebellum predicts the timing of an upcoming movement, utilizes sensory feedback from the current movement, compares ongoing performance to an internal model, and then adapts responses such as force and/or trajectory (Penhune et al., 1998; Zatorre et al., 2007). Schmitz et al. (2003) observed that children with ASD exhibited latency of movement events, indicating over reliance on proprioceptive feedback to maintain postural stability. Bower (1996) suggested that the posterior cerebellar vermis coordinates proprioceptive input from muscle stretch receptors to optimize motor control. If there are cerebellar differences in ASD, the integration and response to feedback may be challenged or require additional accommodation. Since auditory feedback has been utilized to aid in proprioceptive muscular control (Thaut et al., 1999a; González and Yu, 2009; González et al., 2010), rhythmic auditory stimuli may create a feed-forward interaction directly influencing motor output in a predictive way (Zatorre et al., 2007). This would provide the person with ASD an accommodation facilitating more efficient and fluid movement without over-reliance on proprioceptive feedback.

The application of rhythm may serve to facilitate sensorimotor synchronization in autism, but based on other implicated deficits, it may contribute not only to gross motor functioning, but also related perceptual motor responses. One such perceptual motor skill is anticipatory preparation of movement. Gerloff et al. (1998) demonstrated that internal pacing of movement poses higher demands on the motor system than external pacing. Since individuals with autism exhibit deficits in anticipation (Rinehart et al., 2001) and appear to lack sufficient internal cueing, an external auditory rhythmic cue could provide a temporal template for organization of motor output while simultaneously decreasing the demand and increasing efficiency of movement. Auditory rhythmic stimuli can serve as predictable timing cues that influence motor anticipation resulting in the response pattern gradually becoming automatized (Thaut et al., 1999a).

Adams and Chambers (1962) and Schmidt (1968) investigated the automatization process of motor patterns and suggested that anticipation appeared to be “variable depending on the predictability of external response cues,” and temporal and spatial predictability of those cues was most influential on anticipation. Because rhythmic tracking requires predictability of the stimulus, typical participants demonstrated anticipation as their motor responses were slightly ahead of the beat [as cited in Thaut et al. (1999a)]. Patients with cerebellar impairment showed intact rhythmic synchronization and evidenced similar anticipatory responses (Molinari et al., 2007); therefore, an auditory-motor stimulus of rhythm would likely impact anticipatory preparation in movement in persons with autism. Treatment geared toward building an anticipatory means of motor control in autism might then facilitate the development of internal models for motor planning.

Motor planning or praxis is an essential skill for motor function. Studies have shown that persons with autism exhibit a generalized praxis deficit (Mostofsky et al., 2006; Dewey et al., 2007; Dziuk et al., 2007) and that this may be attributed to perceptual motor elements (Vanvuchelen et al., 2007). It has been found that children with autism are not able to translate their motor intention into a global action, but that they program single acts independently from each other (Fabbri-Destro et al., 2009). External cueing of rhythm might lessen the internal demands placed on an individual with autism by providing precise reference intervals at each stage of the movement. This might allow for an increase in fluency and accuracy of movement parameters, as well as organization of the overall movement sequence.

Although rhythm has not yet been studied in this context with persons who have ASD, the above evidence suggests that motor differences observed including planning and coordination of movement might benefit from auditory rhythmic cueing. It is important to note that this is not simply listening to rhythms; rather, interventions involve the application of rhythm at a tempo appropriate for facilitating a movement pattern or increasing motor stability. The development of interventions using rhythm for motor skills may also include other musical elements such as pitch, structure, and dynamics. These elements can further emphasize motor patterns and engage the client in the therapeutic process. Clinical music therapy interventions often involve music with a strong or embedded rhythm. The emphasis is on the temporal aspect; however, melody, lyrics, structure, and style are incorporated for motivation.

Autism is primarily defined with social and communication deficits; however, current literature suggests that movement differences play a part in autism and that this component warrants further investigation. If clinical treatment of autism addressed motor deficits, appropriate therapeutic goals to impact functional change might include motor coordination, motor planning, and functional motor skill development. Rhythmic auditory cueing could be an appropriate technique to provide a predictable structure to stabilize variability in the movement pattern and facilitate a motor plan. Given the current evidence, this is an area where further research is required to better understand the potential impact of rhythm on movement in persons with ASD.