Tourette’s

Chapter #: Tourette’s Syndrome Offers Speed and Coordination

Tourettes Syndrome Defined:
  Tourette syndrome is a neurological disorder characterized by repetitive, involuntary movements and vocalizations called tics. The condition begins in childhood and continues into adulthood. There is no cure for Tourette syndrome, but behavioral therapy can help. Treatment isn’t needed when symptoms aren’t troublesome. Tics often lessen in adulthood. Symptoms of Tourette syndrome include:   Repetitive movements Vocalizations, grunting, coughing, barking Blinking, eye rolling, grimacing Shoulder shrugging Jerking of the head or limbs Jumping, twirling Touching objects and other people.  

Summary

Tourette syndrome, and the closely related spectrum of tic disorders, are inherited neuropsychiatric conditions characterized by the presence of repetitive and stereotyped movements. Tics are elicited by either environmental experiences or internal signals that instruct the basal ganglia to initiate automatic or procedural movements. In most vertebrates, the basal ganglia encode instructions for habitually used sequences of motor movements that are essential to survival. Tic disorders may represent evolved phenotypes with a lower threshold for basal ganglia-directed actions. This may have produced a susceptibility to extraneous tics but also produced fast-acting tactical solutions to immediate physical problems. During periods of nonstop movement, continual foraging, and sustained vigilance, it may have been advantageous to allow subcortical motor commands to intrude into ongoing motor activities. It is clear that the engrams for individual motor responses held in the basal ganglia are selected by converging cortical and subcortical inputs. This form of convergent action selection results in selecting the most contextually reinforced actions. Today people with Tourette’s have tics that seem arbitrary and inappropriate; however, this may be due to the vast discrepancies in reinforcement between the ancestral environment and the modern one. In prehistoric environments, the motor behaviors of individuals with tic disorders may have been appropriate and had ecological relevance in survival and self-promotion.

Tourette Syndrome and Natural Selection

Tourette syndrome (TS) is an inherited neuropsychiatric disorder. It is characterized by sudden, repetitive, nonrhythmic motor movements called tics. Motor tics include unplanned, stereotyped movements such as eye blinking, facial twitching, and head, arm, hand, or shoulder movements. The verbals tics are called phonic tics and include noises, syllables, words, and phrases. Some tics are highly conspicuous, whereas others can be difficult to notice.

Tourette’s is defined as part of a spectrum of tic disorders, most of which start before puberty. Although individuals with TS have been described since antiquity, the systematic study of individuals with tic disorders began in the nineteenth century [1]. Only a few decades ago, Tourette syndrome was considered a rare and bizarre syndrome, most often associated with the exclamation of obscene words (coprolalia), socially inappropriate remarks, mimicking, and derogatory gestures [2]. However, none of these behaviors are universal. In fact, tics that include cussing or obscene words only occur in about 10% of cases [3].

Merely a few decades ago, TS symptoms were thought to be caused by pent, or “repressed” anger, and psychoanalysis was thought to be an effective form of treatment. Today many Tourette’s researchers instead think that Tourette’s represents some kind of malfunction in the neurological systems that ensure that necessary urges are adequately attended to [4]. It is now known that the disorder is neurological in etiology rather than psychological, and symptoms improve when dopamine transmission in the brain is modified. Medications and behavioral therapy are the most common forms of treatment [5]. Although Tourette’s is the most severe of the tic spectrum disorders [1], most cases are relatively mild [5], and many cases go undiagnosed [6]. The severity of tics decreases during adolescence, and pronounced Tourette’s is relatively rare in adulthood [7]. Furthermore, Tourette’s is thought by some to be continuous with normal human variation, and all people are thought to be capable of movements that qualify for the “tic” label [6]. I certainly remember having tic-like behaviors when I was younger. I would feel compelled to make fast movements and twitches for what seemed like no reason.

Between 1 and 10 children per 1,000 have TS; additionally, as many as 1 in one hundred have a tic disorder [4]. This incidence far exceeds a mere chance effect due to high mutation rates (1 in 1,000) and thus may be suggestive of past positive selection [8]. Because TS has a high prevalence and a robust genetic component [4], the persistence of the genes involved suggests an origin in natural history. It presents with similar prevalence rates worldwide [9], indicating that it was established before the first humans left Africa.

Because it presents during the period of fertility, we can assume that natural selection had the opportunity to select against it. Yet, TS exists today as a relatively prevalent disorder. This amounts to an evolutionary enigma commensurate to the one identified for schizophrenia [10]. The present opinion chapter will explore the possibility that the symptoms of tic disorders may be associated, perhaps at low levels, with certain adaptive advantages in specific environments. It is certainly possible that natural selection may have only favored subclinical traits or been advantageous in less unaffected relatives.

Seizure activity, chorea, dystonia, and myoclonus are other movement disorders that probably were not adaptive nor selected by evolution based on their ability to alter behavior adaptively. Unlike tic disorders, these movement disorders are often precipitated by injury, drugs, or relatively rare medical disease states. Tic behavior is more complex and may fit the adaptationist program as it has aspects of contextual responsivity and intentionality. The costs of TS are well known and include constrained mobility, occupational disability, and psychological stress and suffering [11]. The defensive value, however, may be hidden due to discrepancies between the modern and ancestral environments.

Please recall from previous chapters that to determine that a disorder or disease has adaptive qualities that were positively selected in the past, it is important to show that the trait is relatively prevalent, heritable, and that susceptibility varies within a population [25]. These are all true of TS. However, it is also necessary to show how the trait’s purported benefits may have outweighed the costs [13]. It does not appear that individuals with TS would have suffered great hardships or had barriers to reproduction in the ancestral environment. Furthermore, Tourette’s does not adversely affect intelligence or life expectancy [26]. Both children and adults with TS have been shown to be psychologically hardy and, despite the frustrations associated with their symptoms, are surprisingly well-functioning in social, emotional, and behavioral measures [3]. In fact, they are remarkably similar to control children without TS on most psychosocial measures. This suggests that despite the accompanying physical limitations, TS may not necessarily have unduly hampered reproductive success due to psychological or motivational factors.

Movement and Motor Advantages Associated with Tourette Syndrome

Compensating benefits associated with Tourette syndrome have been reported in studies comparing individuals with TS to controls [6]. Georgiou and researchers [27] found that patients with TS, when tested in terms of kinematics, were in certain respects more force efficient than controls and made fewer inefficient cycles of motoric acceleration and deceleration on complicated motor tasks. On average, individuals with TS perform behavioral tests of cognitive motor control more quickly and accurately than their typically developing peers do [28]. Children with TS have a significant processing advantage in judging time intervals [29]. Individuals with TS also exhibit enhanced cognitive control over their oculomotor responses, and increased performance is associated with tic severity [30]. The study authors speculate [31] that the enhanced cognitive control of motor activity seen in TS patients may stem from the constant requirement to suppress tics; however, the enhancements may be inherent to TS.

Individuals with TS have been reported to excel in certain competitive sports [5; 32]. Furthermore, it has been claimed that tics can allow improvisation and extemporization with musical instruments. Patients report that they are physically slower, less coordinated, and have a diminished knack for repartee when they are on medicines that reduce ticcing [33] (although people without Tourette’s taking neuroleptics report this as well). There have not yet been any systematic research efforts aimed at delineating the motor advantages and deficits in individuals with TS, but further research may be illuminative.

When an individual with TS stops making a conscious effort to suppress their symptoms, or if they become emotionally aroused, tics are more likely to emerge [36]. Tics have been shown to decrease in frequency during concentration on an absorbing activity [6]. Another aspect of tics is that even though they are often described as irresistible, they are typically consciously suppressible or at least able to be delayed. Touretters describe these “premonitory urges” as having properties akin to an itching sensation. Like the impulse to scratch an itch, tics can be inhibited only through mental effort and restraint [3]. Given that they can be deliberately suppressed it seems clear that tics would not have compromised reproductive success and survival by bursting forth during extremely inopportune times.

Neurologist and author Oliver Sacks has written about the compensatory advantages of TS. He states that clinical observers of Tourette’s routinely note a peculiar quickness of movement. Sacks [33] also wrote a story about a pilot and surgeon with severe Tourette syndrome whose tics have been documented to go into almost complete abeyance during his operations. A dozen or so M.D.s with Tourette syndrome work quite safely as surgeons [34]. Sacks describes the musician [35], “Witty Ticcy Ray,” in the following way:

“…a weekend jazz drummer of real virtuosity, famous for his sudden and wild extemporizations, which would instantly arise from a tic or a compulsive hitting of a drum, and would instantly be made the nucleus of a wild and wonderful improvisation, so that the ‘sudden intruder’ would be turned into a brilliant advantage (p. 94).”

Many individuals with Tourette’s lose all noticeable manifestations of the “disorder” when singing, dancing, or acting and can remain tic free when moving rhythmically or continuously [33; 32]. From the Darwinian viewpoint, Leckman and Cohen [6] ask whether there might be an advantage in having vulnerability to develop TS. They claim to have made clinical observations that TS patients have a “thinner barrier to stimulation” and may have been more “aware of dangers” in the ancestral past. I find this interesting; however, this chapter will take another perspective and argue that a propensity for tics may have amounted to a form of restlessness that ensured that the individual remained physically and motorically integrated with their immediate environment. During periods of migration and repetitive foraging activities, it may have been advantageous to allow subcortical motor commands to intrude into ongoing motor activities.

TS symptoms may therefore exist on a continuum with two ends: one extreme involving simple, isolated motor tics and vocalizations that are largely irrelevant, seemingly arbitrary, and have the potential to be a nuisance. The other extreme involves the disinhibition of basal impulses, rapid inventiveness, and unhesitating reactivity. Perhaps the isolated and inappropriate tics are a natural tradeoff that occurs when the threshold for activity of the basal ganglia is lowered.

Ticcing disorders may descend from an environment when social propriety mattered far less than speedy reactions. Furthermore, there may have been less social stigma on wild, loose behavior in the ancestral past. Tics often appear as risqué, irreverent, or even antisocial, but this may simply be because the frontal lobe does not filter them. Thus, tics may merely be the striatum’s most appropriate associations untempered by forethought, tolerance, empathy, or compassion.

The Brain in Tourette Syndrome

The mental instructions for discrete movements usually pass through a complex network of cognitive filters in the frontal cortex. The PFC typically either strengthens or inhibits the impulses originating from the dorsal striatum, permitting some and curtailing others. The putamen (which controls automatic movements previously learned by repetition) sends its instructions on to the premotor cortex, which passes its activity on to the adjoining motor cortex. Usually inputs from prefrontal and premotor areas are combined and integrated with inputs from the dorsal striatum in this way and are then sent to the motor cortex. The motor cortex delivers these motor programs to the muscles by way of the spine or cranial nerves. During tics, the frontal cortex fails to inhibit the caudate nucleus and putamen, which lie directly beneath it. In Tourette’s, the putamen is overactive. Furthermore, TS has been associated with a lack of activity in three areas: 1) the dorsolateral prefrontal cortex (concerned with generating appropriate actions); 2) the left basal ganglia (concerned with the control of automatic movements; and 3) the anterior cingulated cortex (an area concerned with focusing attention on actions [37].

A motor movement is generally selected by: 1) external environmental stimuli, or 2) internal stimuli. Either can trigger a memory for a specific motor movement in the striatum. This happens when the memory is converged upon by a set of inputs from cortical and subcortical areas and activated above a certain threshold. In other words, the cooccurrence of a specific set of stimuli, either in the environment or in internally generated thinking, will initiate a complex search function characterized by spreading activation to select the corresponding motor outputs [38]. Thus, even though they may seem arbitrary, tics are chosen with high specificity.

Today individuals with Tourette’s report feeling a sense of reward accompanying their ticcing actions. Reward is associated with high levels of dopamine release, which promotes habit formation in the basal ganglia, increasing the frequency of the action. Thus, dopamine serves to capture and reinforce striatal behaviors engraining these patterns as habitual tics [39]. This process may leave individuals, especially those that are genetically predisposed to Tourette’s, to be vulnerable to maladaptive motor tics when contextually unnecessary responses are captured. In the prehistoric past, humans were responsible for finding or making shelter, protecting their bodies from predators, and foraging for food. These activities determined their reinforcement schedule. Today we rarely do any of these things. What the basal ganglia found motivating in ancestral times was probably very different from what it finds motivating today. In the ancestral past, the motor plans that were converged upon may have been more likely to be advantageous movements rather than extraneous, idiosyncratic ones.

In his book, The Triune Brain in Evolution [40], the late Paul MacLean describes the basal ganglia as the reptilian brain (also referred to as the archipallium or R complex). He describes how it can be taken to represent the dominant mediator of adaptive behavior in reptiles, amphibians, and fish. He describes the basal ganglia, limbic system, and neocortex as three different biological computers linked together, different in structure and chemistry, tens of millions of years apart in provenance, and each with its own representations of time, space, motor repertoire, and subjectivity. He describes their functionality as intermeshing, and independent but not autonomous. Much of his life’s work was dedicated to explicating how the basal ganglia is responsible for the largest proportion of behavior in nonmammalian vertebrates, their learned behaviors, repetitive behaviors, social displays, species-specific master routines, and individual-specific (and idiosyncratic) subroutines. The large size and vast integration of the basal ganglia in humans is clear evidence of its importance in human behavior. Perhaps it should not be surprising that the human gene pool produces phenotypes where this system is granted increased autonomy.   

Stress, Phenotypic Plasticity, and Tourette Syndrome,

In this book, we have seen that the phenotypic characteristics of organisms ranging from plants to mammals have been shown to make various plastic responses to environmental stressors [41]. Stress has been shown to demand variant body types, behaviors, reproductive tactics, and life-history strategies. Epigenetic responses to chronic stress cause the mammalian brain to respond with a number of adaptive adjustments that increase vigilance, threat awareness, and physical responsivity [22,42]. Stressful environments put more pressure on animals to react quickly and efficiently [43]. Most vertebrates, under times of severe or chronic stress, must react quickly and use their muscles vigorously and for sustained periods [44].

We have seen that after extended exposure to stress, higher-order cognitive brain areas are toned down relative to the areas responsible for reflexes, and the execution of procedural movements [44]. Interestingly, there is a strong documented association between stress and TS. This association may suggest that stress causes the expression of genes that lead to increased ticcing behaviors because tic-like behaviors may have been particularly adaptive in a stressful or adverse environment.

Psychogenic stress is known to exacerbate TS symptoms on the order of days, weeks, and months. Psychological stress has been tied closely to onset and has been shown to precede flare-ups. Stress reliably accelerates TS disease progression and worsens symptoms [3]. Tics have been known to increase in frequency due to stress and anxiety [39]. Also, ticcing disorders can be triggered during childhood by a traumatic event. Tic severity [45] and TS diagnosis [46] has been associated with maternal psychosocial stress during pregnancy. This strong association between TS and stress may suggest that an adverse or hostile environment may have favored tics. If TS constitutes a “predictive adaptive response” to stress, then it should be informative for researchers to focus heavily on the molecular pathways that tie stress to TS exacerbation.

Stress is strongly associated with basal ganglia upregulation in mammals, from rats to humans. Memory is multifaceted and different facets are mediated by different brain areas. Explicit memory for movement supports consciously accessible knowledge, such as memory of what one just did or did yesterday. This is mediated by the medial temporal lobe, particularly the hippocampus [47]. On the other hand, procedural or habit memory for movement is responsible for simple stimulus-response associations, such as the memory to stop a car when the light is red, which is mediated by the caudate nucleus [48].

Hippocampus and caudate-based memory systems work in parallel and have been described as cooperative by some and competitive by others [49]. We have seen that studies have found that chronic stress significantly increases activity in the caudate nucleus [50] and improves performance on simple, habitual, and/or well-rehearsed tasks [51; 52]. In both humans and rodents, chronic stress has been associated with a substantial decrease in the use of hippocampal-dependent learning strategies and a dramatic increase in the use of caudate-based learning strategies [53]. It seems that a consequence of chronic stress is to shift away from explicit processing (PFC and hippocampus-dependent) and toward rigid, stimulus-response, implicit processing (caudate and amygdala dependent) [55; 56].

Humans under intense chronic stress have been shown to exhibit improved simple reaction time [57], potentiated reflexes, and increased speed for habitual movements [58]. In fact, Vasterling and collaborators [57] suggest that this heightened behavioral reactivity may represent an evolutionarily-mediated neurobiological response to stress “in preparation for life-preserving action.” A similar type of behavioral disinhibition may have permitted TS individuals to react without deliberately reflecting on their decisions, helping them to escape harm and attain resources quickly and without hesitation. It seems possible that TS is an evolved phenotype intended to adopt a different life-history strategy that allowed affected individuals to react quickly without the normal inhibitory pressures on their reflexes and instincts.

Conclusions

The present chapter concludes that it is plausible that the genes that predispose people to Tourette syndrome, and the spectrum of tic disorders, may have been naturally selected for their role in rapid physical responding. Tics have been conceptualized here as automatic selections from lower brain centers about appropriate tactical movements. This may be associated with the compensating benefits enumerated in Figure 1.

Figure 1

Advantages of Tourette’s and Tic Disorders

  • Reduced inhibitory pressure on reflexes and motor pathways
  • Heightened efficiency in the use of force
  • Reduced reaction time and refined rhythmic activity
  • Increased innate and instinctual behaviors
  • Advanced ability for improvisation or extemporization
  • Increased defensiveness, withdrawal, avoidance, vigilance, and opportunism
  • Stimulus hunger, adaptive restlessness, and unhesitating reactivity

Tic and tic-like behaviors were probably only adaptive in specific contexts. The intrusion of tics may have been most adaptive when they were incorporated into an ongoing series of movements. Tics that emerged as isolated and discrete movements when no other behaviors were being performed, or that were not applied to physical objects in the environment may have been less likely to be adaptive. In other words, tics may have been functional, during more active times, as integrated adjustments to ongoing motor behavior.

The statistical age of highest tic severity is typically between eight and twelve, with most individuals experiencing declining tic severity as they reach adolescence. [59]. In many cases, a complete remission of tic symptoms occurs after adolescence [60, 61]. Why would this epidemiological pattern be so widespread? Is it possible that tic-like behavior is part of a learning arc, benefiting children by helping them to refine coordination and movement patterns?

It will be challenging to determine irrefutably if what we know as TS was an adaptive condition in the ancestral past. The hypothesis presented here is largely exploratory and underspecified, partly due to the need for more related research. The present chapter has made untested assumptions about stress ecology and the nature of striatal cognition in the wild. Most common tics observed in modern populations would probably amount to handicaps in an ancestral environment. They might make an individual unattractive to potential mates, betray one’s location to a predator or waste valuable energy. Common tics like toe crunching, throat clearing, and abdominal tensing would probably have been useless for prehistoric foragers that exhibited them. Moreover, the present hypothesis offers no explanation for chronic tics. However, this type of exploratory writing is generally thought to be progressive as it is well known that analyzing disease states from an evolutionary perspective can integrate seemingly unrelated findings, elucidate pathophysiology, and ultimately refocus clinical research and treatment strategy.

Comparative behavior and neurophysiology could provide insight. Perhaps other species also have an equally low but consistent prevalence of ticcing phenotypes. It would be interesting to see if there are analogs, or possibly homologs of TS in other species. If there were homologs of TS in species closely related to humans, it would be relatively easy to use molecular techniques to show this, given that the genes responsible could be identified. Looking at the evolutionary signatures in the behavioral genetics of TS might tell us more about its possible role as an adaptation. Further kinematic and biomechanic studies comparing individuals with TS to controls on measures of fluidity, efficiency, and speed could help to determine what kinesiological advantages TS individuals have, if any. 

It is possible that today tics are often not contextually relevant because of the artificial nature of the modern environment. Caudate hyperactivity in the ancestral past may have led to the potentiation of important procedural and habitual movements, increasing reliance on action patterns that had proven effective. In modern society, it may simply lead to the intrusion of eccentric responses. The existence of TS may represent natural human variation and may demonstrate that sometimes it was adaptive to allow the basal ganglia and its procedural memories to dominate behavior uninhibited.

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