Autism as a disorder of prediction

1. Insistence on Sameness.

Insistence on sameness (IoS) is a hallmark feature of autism. It is estimated that more than one-third of all individuals on the autism spectrum display some form of IoS (14). This trait may include repetitive thoughts and actions, behavioral rigidity, a reliance on routines, resistance to change, and obsessive adherence to rituals. Underscoring the significance of IoS as an attribute of the autism phenotype, the DSM-5 (15) incorporates IoS into its diagnostic criteria for the condition.

We can draw a compelling link between predictive impairments and insistence on rituals. Past research with diverse populations has shown that environmental unpredictability is strongly correlated with anxiety (16⇓⇓⇓–20). Predictability is a fundamental modulator of anxiety in that reduction in the ability to predict events, even without any associated aversive consequence, enhances anxious responses (21, 22). Anxiety, especially when it is elevated chronically, is known to give rise to ritualistic behavior. These behaviors may be as benign as leg-swinging in school children who are working on a stressful math examination (23) or alarming stereotypies that may cause self-injury (24). Studies with neurologically healthy humans and animals reveal that the ritualistic behaviors that emerge under conditions of unpredictability serve as a calming response to an externally imposed stressor (25, 26). Taken together, these results suggest that rituals and an insistence on sameness may be a consequence of, and a way to mitigate, anxiety arising out of unpredictability.

First-person accounts by individuals on the autism spectrum are consistent with this possibility. For instance, Deborah Lipsky, a board member of the Autism Society of Maine says (27):“I can’t emphasize enough how critical it is to understand that staying on a script is the sole means of keeping anxiety at a minimum. Even the smallest breach becomes a crisis because all we register at that moment is unpredictability. We fear unpredictability above all else because we are out of control of our environment.”

Completing the linkage to ritualistic behavior, Dora Raymaker, director of the Academic Autistic Spectrum Partnership in Research and Education, writes:“The experience of many of us is not that ‘insistence on sameness’ jumps out unbidden and unwanted and makes our lives hard, but that “insistence on sameness” is actually a way of adapting to a confusing and chaotic environment…”

The same argument applies to stimming, a term used to refer to self-stimulating behaviors. The seemingly compulsive need to stim and their oftentimes social inappropriateness raises the possibility that these behaviors might be elaborate involuntary motor ticks. However, parental reports indicate that stimming behaviors are most evident in situations of heightened external stimulation (27), suggesting that stimming may be an anxiolytic response to a chaotic world: an attempt to drown out the influx of unpredictable environmental information by self-generated periodic and, hence, more predictable information. Consider this first-person account from Temple Grandin:“When I did stims such as dribbling sand through my fingers, it calmed me down. When I stimmed, sounds that hurt my ears stopped. Most kids with autism do these repetitive behaviors because it feels good in some way. It may counteract an overwhelming sensory environment…”Temple Grandin, Autism Asperger’s Digest, 2011

To summarize, a parsimonious interpretation of the reliance on rituals and stimming behaviors observed in autism is that they emerge from, and represent attempts to minimize, the consequences of unpredictability. They allow for a proactive imposition of “sameness” on an otherwise overwhelming environment.

2. Sensory Hypersensitivities.

It is estimated that nearly 90% of all children on the autism spectrum suffer from sensory abnormalities, often hypersensitivities, to stimuli that a neurotypical individual could easily ignore (28). These hypersensitivities cannot be explained as outcomes of abnormally enhanced sensation (29⇓–31).

An alternative account of hypersensitivities comes from considering the complementary question: How do neurotypical individuals avoid being overwhelmed by sensory stimulation? A key role in suppressing sustained stimulation is played by our ability to habituate. A direct corollary is that reduced habituation reduces stimulus suppression. Immersion in an unrelentingly salient stimulus is known to be anxiogenic, as studies of the consequences of sensory bombardment have shown (32). Thus, aversion to environmental sounds that individuals with autism exhibit could arise from reduced habituation (33). However, this account begs the question, what kinds of factors might reduce habituation in autism?

A key determinant of habituation is stimulus predictability. For typically developing subjects, predictability of a sequence is directly proportional to the extent of habituation it induces (22, 34⇓–36). Reduction in discerning predictive relationships between events in a stimulus sequence would reduce a person’s ability to predict the onset of the next event. Such a lack of predictability would compromise habituation and lead to hypersensitivity. Support for this idea can be found in a distasteful domain—torture techniques. Several studies have demonstrated that unpredictability of stressors is one of the key aspects of torture and leads to the development of anxiety, fear, and aversion (19, 37). “Acoustic bombardment” has long been used as an instrument of torture. Unfamiliar, and hence unpredictable, music is found to be especially effective (38). Tying this back to the domain of autism, the PIA hypothesis suggests that an endogenous predictive impairment causes environmental stimuli to appear more chaotic, leading to reduced habituation and hence greater stress.

3. Difficulties in Interacting with Dynamic Objects.

The dynamic world presents challenges to those with autism. The Autism Wandering and Elopement Initiative collaboration states that two in three “elopers” (autistic children who attempt to run away) have a close call with a traffic injury (39). According to the Center for Advanced Infrastructure and Transportation at Rutgers University, the vast majority (more than 75%) of people on the autism spectrum cannot drive (40). In first-person accounts, individuals with autism describe the difficulties they had as children engaging in dynamic games on the playground (41). These reports are puzzling given that moving objects are not inherently aversive to those with autism. Indeed, many children on the spectrum are especially drawn to moving objects, enjoy video games (42), obsessively set objects in motion, and even engage in visual stimming that generates movement. What then underlies autistic individuals’ difficulties with dynamic objects?

It is instructive to examine the specific nature of these difficulties. Several studies have shown that basic motion detection and direction perception thresholds are largely unimpaired in autism (43⇓–45). However, to interact with a dynamic object, there is a crucial step beyond detection: anticipating where the moving object is likely to be so as to plan one’s motor movements appropriately to intercept/avoid the object. Even the seemingly simple task of keeping track of a moving object requires such anticipation; it is a manifestation of online Markov model estimation, as a visual temporal sequence unfolds. Computational systems for dynamic object tracking rely on predictive techniques such as Kalman filtering (46). These systems demonstrate that a key consequence of impaired prediction is errors in online position estimation. Transposed to the real world, this impairment would render seemingly straightforward tasks like avoiding a car or even catching a ball difficult for a person with autism.

Consider the following first person account:Throwing a ball was not a problem. However, I couldn’t catch a ball until I was Age 13! I was criticized by my father about my ability, or lack of, to work with my hands.(Jon Evans on www.DisabilityScoop.com)

Given the prediction-reliant nature of tasks requiring interactions with dynamic objects, the PIA hypothesis provides a plausible account of the difficulties that individuals with autism encounter in such settings.

4. Difficulties with Theory of Mind.

Theory of mind requires the ability to ascribe invisible causes to observations about a person by connecting past history with current behavior. Deducing why a person acted a certain way, or anticipating how a person is likely to act, requires the estimation of a conditional probability: Given a certain observation about a person and the circumstances, what are the likely precursors leading up to them, and in a similar vein, what are the next stages in their evolution? In this sense, Theory of mind is inherently a prediction task—given an observation, one has to postdict or predict its antecedent or subsequent states, i.e., estimate P(past history | current behavior) or P(future actions | current observations). Given the often-weak relationships among history, present observations, and future behavior for humans in social settings, these states involve the estimation of challenging probabilities and, hence, are especially vulnerable to impairments in predictive ability. Impairments in Theory of mind are a prominent correlate of autism (47).

Impairment in prediction would render an observer unable to situate current observations about a person in the context of their antecedents or likely future states. The observer, in effect, will be constrained to interpret observations “in the moment.” Such interpretations would manifest themselves as being literal, in that they describe what is happening from moment to moment, but are not influenced by past history and do not presage future events. The minimalistic movies of Heider and Simmel provide an interesting case in point (48). Having access to a probabilistic conditional relationship between observed movement patterns and potential histories, neurotypical individuals are able to ascribe causes to the former. The fact that these causes happen to be social in nature is likely happenstance; the social account is simply a better predictor of the observations than other historical accounts. An autistic individual, not having access to such predictive relationships, is constrained to interpret behaviors without any motivating history, social or otherwise (49).

In this way, the PIA hypothesis provides a simple account of the difficulties autistic individuals experience with theory of mind and other abstractions, which require the use of learned interevent relationships to read more into an observation than the basic sensory signal offers.

5. Islands of Proficiency.

Individuals with autism have been reported to show preserved, or even enhanced, abilities relative to neurotypical controls in several domains (50). These islands of proficiency include mathematics (51), static form coherence (52), visual search (53, 54), block design tasks (55), calendar calculations (56, 57), musical performance (50, 58), and drawing abilities (59, 60). These seemingly distinct domains share an important characteristic. Most of them, especially mathematics calendar calculations and music, are strongly rule-based, and, thus, minimize uncertainty of outcomes. Furthermore, with the exception of music, they are static, thereby obviating the need for prediction over time. If the prediction systems of the brain are differentially affected in autism, then one can expect that the skills left largely untouched would be the ones that are deterministic and where good performance does not depend on estimates of temporally unfolding conditional probabilities.

An examination of studies of preserved or enhanced proficiency in music (61, 62) reveals that the observed high performance is typically in replication. The reports further note that such factors as perfect pitch, prodigious memory, and extensive rehearsal, while contributing to the extraordinary skill set, are not sufficient to explain it (50, 58, 60). Detailed studies of musical savants with autism reveal that the basis for exceptional recall and performance, including improvisation, is familiarity with the structure of music and, thus, depends on adherence to rules (63).

As the foregoing discussion suggests, the PIA hypothesis provides a parsimonious account of some notable aspects of the autism phenotype. We next consider some empirically testable predictions this hypothesis makes about other traits that “should” be observed in individuals with autism.

1. Hyperplasticity.

An important outcome of reduction in predictive abilities is a heightening of the perceived novelty of environmental stimuli. This enhanced novelty has a potentially interesting consequence on learning. It is known that activity in the brainstem and basal ganglia is modulated by novelty (64). Furthermore, significant evidence suggests that these structures play an important role in modulating learning (65, 66). Given the elevation of novelty due to impaired predictive skills, one would expect hyperactivation of the brainstem and basal ganglia in individuals with autism. Hyperarousal of these structures would, in turn, be expected to lead to hypermalleability of learning; current exposure would have disproportionate weight and supersede earlier experience, constituting a kind of “hyperplasticity.” Notably, such hyperplasticity would, in turn, further impair instance aggregation and, thus, an accurate estimation of probability values. Interestingly, precisely such hyperplasticity has been reported in mouse models of autism (67).

2. Changes in Striatum, Basal Ganglia, and Cerebellum.

In neurotypical individuals, the key brain loci that have been implicated in prediction are basal ganglia (68, 69), striatum (70, 71), anterior cingulate (72), and cerebellum (73, 74). If predictive abilities are affected in autism, then we would expect these regions of the brain to be especially implicated. Indeed, the emerging picture from recent neuro-imaging, postmortem, and animal-model studies is that atypicalities in these regions are associated with autism (75⇓⇓⇓⇓–80).

3. Reduced Appreciation of Humor.

A key component of humor is violation of expectation (81, 82). This implicitly requires the listener to have a prediction of how a given sequence is likely to unfold. A benign deviation from that prediction often constitutes a humorous outcome (82). In the absence of a strong prediction, a violation is harder to define and detect. Hence, opportunities for perceiving humor in narratives or observations are diminished. With this logic, the PIA hypothesis predicts that the sense of humor of individuals on the autism spectrum would be diminished or at least altered relative to that of neurotypicals.

Although systematic research on how autism affects the sense of humor is still in its infancy, some evidence supports this prediction. In describing his patients, Hans Asperger had noted that “an essential characteristic of these children is their humorlessness. They do not understand jokes…” (83). More recent studies (84, 85) have also documented these observations. It is particularly interesting to note Emerich et al.’s (86) finding that adolescents with autism had special difficulty “handling surprise and coherence within humorous narratives.”

4. Reduced Motor Anticipation.

Starting from a very early age, much of human motor behavior is anticipatory in nature. Whether it is adopting appropriate foot placement and body-posture while walking on uneven ground, or mouth shaping during speech articulation, there is extensive evidence for motor anticipation (87⇓–89). The PIA hypothesis predicts that motor anticipation would be reduced in individuals with autism. The evidence so far is generally consistent with this prediction (90, 91). Even in his initial case reports, Kanner (92) noted poor anticipation on the part of autistic children to being picked-up by their parents. More recently, in a retrospective analysis Brisson et al. (93) have reported anticipatory failure during feeding situations in infants between 4 and 6 mo old who were later diagnosed as having autism. Fournier et al. (94), among others (95, 96), have found poor postural control in children with autism. Given that anticipatory processes have been implicated even in the maintenance of muscle tone (97), the PIA hypothesis might also help account for some aspects of hypotonia observed in children with autism.