Hypoentropic Dynamics: a Hypothesis for the Mechanism of the Autism Spectrum Disorders

Ramon Cererols, e-mail: rcererols@gmail.com

Freely available at: http://pairal.net/asperger/dhe.php (May 2012) Abstract
Autism spectrum disorders are characterized by a very diverse set of manifestations, which no existing theory manages to explain in its entirety. It is therefore reasonable to think that there is an underlying global mechanism, which requires applying to the brain the study methods of complex dynamic systems. The entropy level of the brain determines the type of emergent computation and, as a result, its respective ability for deterministic and heuristic processing. This article proposes the hypothesis that the cognitive profile of autism spectrum disorders is due to a brain structure that generates a hypoentropic dynamics. We argue that the hypothesis is entirely consistent with all seven groups of symptoms and manifestations commonly observed and we refer to recent studies that suggest lower entropy in people with autism spectrum disorders. The model of hypoentropic dynamics provides a new approach to research, diagnosis and treatment of autism.

Keywords
Autistic Disorder. Behaviour. Cognition. Entropy. Nonlinear Dynamics. Phenotype. Theory of Mind.

Introduction
Pervasive developmental disorders (PDD) share three basic diagnostic criteria: a) qualitative impairment in social interaction, b) qualitative impairments in communication, and c) restricted, repetitive, and stereotyped patterns of behaviour, interests, and activities (1). Typically, these core symptoms are accompanied by other signs (sensory, cognitive, motor, etc.), but all of them have in each case a different intensity that depends on personal factors. This phenotype variability has led to consider PDD as a group of distinct disorders (autistic disorder, Asperger disorder, childhood disintegrative disorder, Rett's disorder and pervasive developmental disorder not otherwise specified), but there is an increasing tendency to consider the uniqueness of the whole spectrum. In this sense, the current proposal for the new version of the Diagnostic and Statistical Manual of Mental Disorders (DSM-5), scheduled for 2013, is to subsume all of them under the name of autism spectrum disorders (ASD) (2). Complexity of symptoms, coupled with the lack of biological markers and of a definitive aetiology has led researchers to develop several theories to explain the cognitive mechanism of ASD. Those that have gained greater acceptance are: a) deficits in theory of mind (3), b) weak central coherence (4), c) executive dysfunction (5) and d) imbalance in empathizing systemizing or extreme male brain (6). Each one of these theories explains a subset of symptoms of ASD, but none explains all of them, so it can be considered that: either the ASD are not due to a deficit in a single cognitive module, but several simultaneously (7), or there is only one more basic and comprehensive mechanism that explains all. It is important to highlight that, despite the observed phenotypic variability, professionals with many years of experience tend to perceive a common cognitive style above the specificities. Thus, Professor Uta Frith, who has worked for more than 40 years in the investigation of ASD and has written several books and hundreds of articles, deems interesting to

find out the cause of this intuition and thinks it is due to the existence of something unique and ubiquitous in autism, which must be at a cognitive level (8). The aim of this paper is precisely to propose a hypothesis for this mechanism. For that it is convenient to start fixing the concepts that underpin the argument.

Concepts used
Entropy
Although born in the nineteenth century thermodynamics to explain energy flows, the entropy concept was later extended to other very different areas, as information theory, evolution, biology, economics and quantum mechanics. We can define entropy in a simple way by saying that it is a measure of the degree of disorder in a system. Second law of thermodynamics states that in any closed system, with no interaction with the outside, the total amount of entropy always tends to increase.

Complex dynamical systems

When the elements of a whole do not interact with each other, properties of the whole are simply the sum of the properties of the parts. For example, the behaviour of one litre of water is the same as that of any of the approximately 31025 molecules of H2O that compose it. Its grouping does not add anything qualitatively new. In contrast, when elements of a set interact with each other and with the environment, as in living organisms, in them emerge new properties that were not in the original components and neither can be derived linearly from them. Then the system acquires its own identity and we say that it is a complex dynamic system (CDS). The complexity of a CDS is born out of a large number of very simple individual components with strong relationships and feedbacks, none of them acting as coordinator. The generated structure has various levels of abstraction between which there are two-way causal relationships (9). Two typical examples are an ant colony and a human brain. In both cases 1

the individual elements (ants and neurons) have relatively simple behaviour, but from their interaction systems emerge with complex and self-organizing properties, hence the importance attached to the application of network theory in neuroscience (10).

Adaptation
For a CDS to be able to respond to changing environmental conditions, it must combine two seemingly contradictory conditions: that its components are sufficiently structured to function as a whole, and at the same time each of them has sufficient autonomy for its operation. Both extremes may be represented by a crystal (fully ordained but completely still) and a gas (in which the molecules move wildly in all directions). Somewhere in between there is a close critical zone known as the "edge of chaos" in which the system acquires its ability to adapt (11) (Figure 1).

Adaptive landscapes
Adaptation is the execution of real-time computational processes that constantly respond to the environment by modifying its internal state to move it to new equilibrium conditions (12). If we consider the map of all possible states, we see that each system has a tendency to stabilize temporarily in specified areas (points, curves, or more complex shapes) that for this reason are called attractors. The history of the system is therefore a path through the attractors, triggered by external conditions and internal dynamics. One way to represent this phenomenon is to imagine the map of states as an undulating surface (the adaptive landscape) on which a moving ball represents the system state at any particular time. The grooves of varying depth are the attractors to which the ball tends. External changes shake the landscape causing the ball to jump from one to another attractor, depending on the intensity and direction of the impulse, and depending on the shape of the terrain in the area close to the current position (13).

other levels through biology, physiology, genetics, biochemistry, etc. Each discipline is more appropriate for a given level of abstraction (it would be impracticable to try to deduce animal behaviour from their molecular composition) but sometimes the investigation of certain phenomena observed at a level requires the study of other layers. This is the case in the brain. Since the second half of the nineteenth century, with the discovery by Broca and Wernicke of the areas associated with language, has dominated a Cartesian reductionist view that attempts to explain cognitive phenomena with functions independent of each other, located in specific areas of the brain. This approach has proved useful for advancing knowledge in the brain and for the study of a number of anomalies and disorders. But this perspective is insufficient to understand certain emergent properties at the system level (14-17). An example of this is the increasingly global view of memory (18-19).

Cognitive style
Brain development is dependent on many genetic and epigenetic causes that model the forming vectors of the various components and determine neuronal growth and their distribution and connection. For example in ASD there is more brain growth in the early years (20), a higher concentration of minicolumns (21), and lower long-distance connectivity (22). The types of networks generated and the degree of synaptic activity determine the overall computational properties of the resulting CDS, or, which is the same, the person's cognitive style, which will manifest behaviourally in a way that will be interpreted, depending on the situation, as a way of being or as the expression of a disorder (Figure 2).

Figure 2. Cognitive style, determined by the computational properties of the CDS, is a consequence of the biological effects caused by genetic and epigenetic factors, and manifests itself in interactions with the environment (observed behaviours).

Processing modes
The exact point in whom a CDS is located within the critical zone determines its mode of computational process, i.e. the way it responds to external stimuli: its cognitive style. If it is close to the area of order, of low entropy, it will be mainly deterministic, whereas if it goes next to the area of disorder, of high entropy, it will be more and more heuristic (Figure 3). Each of these two processing modes presents distinct characteristics: a) Deterministic computation uses fixed rules algorithms, which are executed step by step in order to obtain the exact solution of a problem. When the problem is complex or the rules are not explicitly defined, the calculation can be very slow or even

Figure 1. Complexity of a system increases as we move away from the ends corresponding to the minimum and maximum entropy. Adaptive capacity of a CDS is obtained in a narrow middle (the "edge of chaos").

Development of the hypothesis

Cognition: from reductionism to holism
A key feature of CDS is to present various levels of organization that can be studied and interpreted (almost) independently by different sciences. For example, an ecosystem can be viewed as a whole through ecology, and at

b)

impossible. The same problem is always solved in the same way and gets always the same result. Heuristic computation relies on induction from experience, and from the creation of hypotheses and the method of trial and error. In this way it obtains quick solutions to complex problems, but the results are only approximate and often incorrect. The same problem can be solved each time differently, getting different results.
Figure 4. The transition from one to other attractor is easy in a highentropy adaptive landscape (gently undulating) but is more difficult in a low-entropy (with deep and isolated grooves).

Proposed hypothesis
The hypothesis I propose in this paper is that the symptoms of ASD are due to a low-entropy brain system, close to the area of order of the CDS, which generates a global cognitive style essentially deterministic, with the following basic consequences: a) The resulting fitness landscape has few deep grooves (wells) separated from each other by broad plains. This causes the system to remain for a long time in a certain behaviour, unable to adapt quickly to changes, since the jump from one to another attractor requires high energy consumption (Figure 4). b) Due to the broad plains between the grooves, when an enough intense external stimulus cause gets the system out of the hole, it rests for a certain period in an unstable state until it falls into a new well. c) This cognitive style presents deficits in all those functions that cannot be solved in a deterministic way, and therefore require a heuristic process. For this hypothesis to be plausible it should be consistent with all the symptoms and characteristics usually observed in ASD, and also it should match experimental data about lower entropy in brain activity of people with ASD. These two points are presented in the following sections.

Consistency with observed symptoms

Deficits in social interaction
Social interaction requires: a) the ability of attributing mental states to oneself and others, and understanding that beliefs and intentions of other people may be different from your own what is known as theory of mind, and b) apply this theoretical capacity in interactive practice effectively and efficiently. This can be summarized by saying that the two necessary skills for social interaction are: building internal models of self and others, and switch quickly between these different models in each new phase of the interaction. In people with ASD social interaction is difficult because: a) The construction of mental models is a heuristic process, involving the creation of hypotheses from the perception of partial abstract patterns and its constant adjustment. b) The fast switching between the various mental models requires a highly flexible system, capable of rapid change with reduced energy costs.

Restricted and repetitive behaviour and activities, difficulty for multitasking

This group of symptoms is directly explained by the shape of the fitness landscape, with deep wells from which it is difficult to leave. Its effects are manifested at different time scales: a) At a small time scale from seconds to hours the same activity repeats continually. b) At a longer time scale from weeks to years daily activities are always executed following the same procedures, and there are obsessive recurrent interests. c) It is hard to execute several tasks simultaneously, because this requires constant switching between them.

Difficulties of abstraction, attention to detail over the whole

Figure 3. The computational capacity curve of Figure 1 is actually the sum of the two shown here for deterministic and heuristic cognition, with their maximums displaced respectively to the zones of low and high entropy.

People with ASD show frequently a lack of cognitive coordination: some mental skills are below average while others may show a much higher capacity. These differences are often related with priority attention to detail, due to difficulties in obtaining the idea of the whole (Gestalt) (23). For example, they can possess a large vocabulary but have difficulty understanding figurative speech or meaning in context; or have great memory for numbers and dates, but little for faces, difficulty in extracting general concepts from cases, difficulty in grasping the implicit rules of social activity; and less ability to discriminate a conversation in a noisy environment (24).

The problem of obtaining the meaning of the whole from its parts is cognitively equivalent to the creation of the internal model of a person from successive observations of her individual actions. As seen in the section on social interaction, this requires a heuristic process and a flexible adaptive system.

emotional instability in the stages of change (in which an obsessive interest can be replaced by another).

Specific preferences
Preferred activities for people with ASD will be those that best suit their deterministic processing: technological professions in which the basic elements are well-defined rules, research activities that require the collection and management of large amounts of data, or other activities like music, which structure and organize distinct elements that are combined according to criteria of harmony and rhythm.

Poor motor coordination

Despite a normal appearance, many people with ASD have a poor motor coordination (problems with gymnastics and sports, less agile and graceful movements, dance, rhythm track), often exacerbated in stressful situations (25). Psychomotricity requires a flexible CDS, able to adapt easily to the environment, as evidenced by the difficulty of building a robot that can walk on uneven surfaces. In a low adaptive system movements are mechanical and not very functional (26).

From savantism to low IQ

The proposed scenario also explains how one disorder can produce savantistic skills in some people and low IQ in others, or even sometimes simultaneously (27). As stated above, a CDS offset towards the low entropy zone is specially equipped for deterministic cognition, in which it gets a high level that on special occasions can reach the savantism. But if the offset is too large, the CDS will begin to leave the critical region and thus the area of computing. So the system, which largely lacked the heuristic process, will also lose a rather large part of the deterministic process, which will cause a low IQ.

Lack of creativity and imagination, poor response to the unexpected

These are two aspects of the same problem: the difficulty to change one's mental state, which can be considered from two aspects: a) Change of internal origin: A low-entropy CDS must generate intense internal activity to get out of an attractor, so it is unlikely to create (imagine) patterns different from the current ones. b) Change of external origin: When an unforeseen event pushes the system out of a stable well, until reaching another it remains in an unstable plain, causing a period of imbalance and confusion. At a short timescale this produces poor response to any incident to break the routine. On a broader scale there are periods of

Comparison with existing theories

To conclude this section, Table 1 shows the degree of coherence of the various theories (theory of mind, weak central coherence, executive dysfunction, and empathizing / systematizing) with each group of symptoms. As seen, the only one consistent with all of them is the hypothesis of hypoentropic dynamics, which instead of seeking the explanation in a specific cognitive module, is based on the overall cognitive style.

Table 1 Degree of alignment of various theories with the observed symptoms ToM=Theory of mind; WCC=Weak Central Coherence; ExD=Executive Dysfunction; E/S=Empathizing/Systemizing; HED=Hypoentropic Dynamics (++ highly coherent; + partially coherent) Symptom groups Social interaction deficits Restricted and repetitive behaviour and activities, difficulty for multitasking Difficulty of abstraction, attention to detail rather than the whole Poor motor coordination Lack of creativity and imagination, poor response to unforeseen Specific preferences From savantism to low IQ ToM ++ ++ ++ + + + + ++ ++ WCC ExD + ++ E/S ++ ++ HED ++ ++ ++ ++ ++ ++ ++

Match with experimental data

Direct measurement of entropy
For some years now, there is a method for measuring entropy suitable for the study of biological signals: the multiscale entropy analysis (28-29), which has been used particularly for the study of cardiac abnormalities (30-31). Recently, it has been applied to the measure of brain entropy in people with ASD, and the results are consistent with the hypothesis of hypoentropic dynamics. A study published in February 2011 analyses electroencephalographic data at rest of children between 6 and 24 months, and shows that the high-risk group (defined as having an older sibling with ASD) has a multiscale entropy significantly lower than the control group (32). Another study published in June 2011 compared the EEG complexity, measured with multiscale entropy, among a group of adults with ASD and another group of control, making social and non-social tasks. In both cases, the ASD group showed a smaller EEG complexity in parietal and occipital regions. Furthermore, both groups showed a greater complexity during social tasks, which confirms that these require a higher level of entropy for its realization (33).

b)

Measurement of process dynamics

Possible causes of hyper reactivity to certain sudden or unusual sounds in people with ASD were also studied by exposing a group of participants with ASD and a control group to uniform sound sequences interspersed at random with a different sound. Response times were significantly slower in the ASD group, which shows the difficulty of adaptation typical of the hypoentropic dynamics (34).

Weak Central Coherence. Poor performance of heuristic processes hampers the creation of the model of the whole from parts and context. c) Executive Dysfunction. Low entropy implies resistance to change mental models and schemes, and therefore difficults planning and implementation of the actions necessary to adapt to new situations. d) Empathizing-Systemizing: Low entropy increases the performance of deterministic processes systemizing and decreases heuristic ability empathizing. Moreover, theories b) and c) are usually attributed to a reduction in long-distance connections in the brain, so reducing the transfer of information between different areas. Precisely the degree of effective connectivity between parts of the brain can be measured by the amount of transferred entropy (35). Finally, one can consider in which way the model of hypoentropic dynamics can help research, diagnosis and treatment of ASD: a) Research: It would open new avenues of research, from a radically different viewpoint. Furthermore, having a specific metric, it would be easier to analyse the complex influence of the various combinations of genetic and epigenetic factors. b) Diagnosis: A biometric indicator applicable from the first months of life could be available. c) Treatment: Once known the relationship between the factors that contribute to the entropy change, it would be possible to intervene in any of them to compensate the negatives.

Conclusion
Despite the remarkable advances in our knowledge of ASD made in the seven decades passed since the original works of Leo Kanner and Hans Asperger, there is still a lack of a theory which provides coherence to the different and seemingly unrelated behaviours commonly observed. The intuition of something unique and ubiquitous in autism, as expressed by Uta Frith (8), is useful to professionals who have obtained it with their experience, but to be useful for advancing in ASD research, it is necessary to concretize this intuition in a cognitive mechanism that defines the disorders unitarily and explains the overall disorder symptoms. Here, as in the field of particle physics, we need to find a model that unifies the various existing theories. Since these theories attribute ASD characteristics to different specific cognitive functions, any unifying attempt must be found on an underlying level, in that subtle limit at which biology and psychology come into contact, where the overall cognitive style that permeates all modules is defined. The hypoentropic dynamics hypothesis proposed in this article is offered as a first candidate for this unification. In the previous two sections it has been shown that it is consistent with the observed symptoms and coincides with recent experimental results. It is interesting to point now, even briefly, how the hypoentropic dynamics encompasses the four theories: a) Theory of Mind. Low entropy difficults heuristic processes that are needed to create mental models of other people, and reduces the flexibility required for an agile social interaction.

Acknowledgements
I would like to express gratitude to Dr. Josep Artigas and Dr. Isabel Paula for the encouragement that they have always provided me, and for their constant review, suggestions and comments to the progressive versions of this document.

References
(1). American Psychiatric Association. Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington: American Psychiatric Association; 2000. (2). Casteel B, Valora J. DSM-5 Proposed Revisions Include New Category of Autism Spectrum Disorders. In: APA DSM-5 Development. [Accessed: 12-10-2011]: Available at: http://www.dsm5.org/Newsroom/Documents/Autism%20Release% 20FINAL%202.05.pdf (3). Baron-Cohen S, Leslie AM, Frith U. Does the autistic child have a "theory of mind"?: Cognition 1985; 21(1): 37-46. (4). Frith U. Autism: explaining the enigma. Oxford UK: Blackwell Publishing; 1989. (5). Ozonoff S, Pennington BF, Rogers SJ. Executive function deficits in high-functioning autistic individuals: relationship to theory of mind. J Child Psychol Psychiatry 1991; 32(7): 1081-105. (6). Baron-Cohen S, Hammer J. Is autism an extreme form of the "male brain"? Advances in Infancy Research 1997; 11: 193-217. (7). Pennington BF. From single to multiple deficit models of developmental disorders. Cognition 2006; 101(2): 385-413. (8). Frith U. Why I am obsessed with this cognitive thing. In: SFARI Simons Foundation Autism Research Initiative. [Consulted 27-112011]: Available at: https://sfari.org/news-andopinion/viewpoint/2011/uta-frith-why-i-am-obsessed-with-thiscognitive-thing (9). Juarrero A. Dynamics in action: intentional behaviour as a complex system. Cambridge, MA: MIT Press; 1999.

(10). Sporns O. Networks of the brain. Cambridge, MA: Massachussets Institute of Technology; 2011. (11). Langton CG. Computation at the edge of chaos: phase transitions and emergent computation. Physica D 1990; 42(1-3): 12-37. (12). Bertschinger N, Natschlger T. Real-time computation at the edge of chaos in recurrent neural networks. Neural Comput 2004; 16(7): 1413-36. (13). Wright S. The roles of mutation, inbreeding, crossbreeding and selection in evolution. In: Proceedings of the VI International Congress of Genetics, 1932: 356-66. (14). Sauer U, Heinemann M, Zamboni N. Getting closer to the whole picture. Science 2007; 316(5824): 550-1. (15). Heylighen F, Cilliers P, Gershenson C. Complexity and philosophy. In: Bogg J, Geyer R. Complexity, Science and Society. Oxford: Radcliffe Publishing; 2007. (16). Nunez PL. Brain, mind, and the structure of reality. New York: Oxford University Press; 2010. (17). Damasio AR. Time-locked multiregional retroactivation: a systemslevel proposal for the neural substrates of recall and recognition. Cognition 1989; 33: 25-62. (18). Fuster JM. El paradigma reticular de la memoria cortical. Rev Neurol 2010; 50(Supl 3): S3-10. (19). Damasio AR. Self comes to mind. New York: Pantheon Books; 2010. (20). Courchesne E, Pierce K, Schumann CM, Redcay E, Buckwalter JA, Kennedy DP, et al. Mapping Early Brain Development in Autism. Neuron 2007; 56(2): 399-413. (21). Buxhoeveden DP, Casanova MF. The minicolumn hypothesis in neuroscience. Brain 2002; 125: 935-51. (22). Courchesne E, Pierce K. Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 2005; 15: 225-30. (23). Happ F, Frith U. The weak coherence account: detail-focused cognitive style in autism spectrum disorders. J Autism Dev Disord 2006; 36(1): 5-25.

(24). Alcntara JI, Weisblatt EJL, Moore BCJ, Bolton PF. Speech-in-noise perception in high-functioning individuals with autism or Asperger's syndrome. J Child Psychol Psychiatry 2004; 45(6): 1107-14. (25). Attwood T. The complete guide to Asperger's syndrome. London: Jessica Kingsley Publishers; 2007. (26). Thelen E, Smith LB. A dynamic systems approach to the development of cognition and action. Cambridge: MIT Press; 1994. (27). Scheuffgen K, Happ F, Anderson M, Frith U. High intelligence, low IQ? Speed of processing and measured IQ in children with autism. Dev Psychopathol 2000; 12: 83-90. (28). Costa M, Goldberger AL, Peng CK. Multiscale entropy analysis of complex physiologic time series. Phys Rev Lett 2002; 89(6): 068102. (29). Seely AJE, Macklem PT. Complex systems and the technology of variability analysis. Crit Care 2004; 8(6): R367-84. (30). Costa M, Goldberger AL, Peng CK. Multiscale entropy analysis of biological signals. Phys Rev E Stat Nonlin Soft Matter Phys 2005; 71(2 Pt 1): 021906. (31). Hanumantha Rao TVK, Ravindran G. Entropy estimation of heart rate variability and computation of its multiscale entropy. Eur J Sci Res 2010; 47(4): 517-30. (32). Bosl W, Tierney A, Tager-Flusberg H, Nelson C. EEG complexity as a biomarker for autism spectrum disorder risk. BMC Med 2011; 9(1): 18. (33). Catarino A, Churches O, Baron-Cohen S, Andrade A, Ring H. Atypical EEG complexity in autism spectrum conditions: A multiscale entropy analysis. Clin Neurophysiol 2011 Jun 3. [In press]. (34). Roberts TPL, Cannon KM, Tavabl K, Blaskey L, Khan SY, Monroe JF, et al. Auditory magnetic mismatch field latency: A biomarker for language impairment in Autism. Biol Psychiatry 2011; 70(3): 263-9. (35). Vicente R, Wibral M, Lindner M, Pipa G. Transfer entropya modelfree measure of effective connectivity for the neurosciences. J Comput Neurosci 2011; 30(1): 45-67.