Enhanced habit formation in Tourette patients explained by shortcut modulation in a hierarchical cortico-basal ganglia model

Abstract

Devaluation protocols reveal that Tourette patients show an increased propensity to habitual behaviors as they continue to respond to devalued outcomes in a cognitive stimulus-response-outcome association task. We use a neuro-computational model of hierarchically organized cortico-basal ganglia-thalamo-cortical loops to shed more light on habit formation and its alteration in Tourette patients. In our model, habitual behavior emerges from cortico-thalamic shortcut connections, where enhanced habit formation can be linked to faster plasticity in the shortcut or to a stronger feedback from the shortcut to the basal ganglia. We explore two major hypotheses of Tourette pathophysiology—local striatal disinhibition and increased dopaminergic modulation of striatal medium spiny neurons—as causes for altered shortcut activation. Both model changes altered shortcut functioning and resulted in higher rates of responses towards devalued outcomes, similar to what is observed in Tourette patients. We recommend future experimental neuroscientific studies to locate shortcuts between cortico-basal ganglia-thalamo-cortical loops in the human brain and study their potential role in health and disease.

The contribution of the basal ganglia and cerebellum to motor learning: A neuro-computational approach

“…After a decision about the target object is determined by the premotor loop, the reaching action does not need further information about those decisions made by the earlier loops. As we have already shown how such a set of decisions could be learned by dopamine-modulated plasticity [ 44 , 71 ], we focus here on the motor loop only and how a motor goal is transformed into a concrete action and its final execution.…”

Immp2l knockdown increases stimulus-driven instrumental behaviour but does not alter goal-directed learning or neuron density in cortico-striatal circuits in a mouse model of Tourette syndrome and autism spectrum disorder

“…Furthermore, changes in size of the caudate (i.e., DMS) correlate with severity of tics, repetitive behaviours and compulsions (Bloch et al, 2005; Langen et al, 2009). In addition, when tested using translation versions of the procedures used in the current study, individuals with ASD displayed reduced goal-directed learning as their actions were not determined by outcome value, and individuals with GTS showed enhanced habits and an over-reliance on stimulus-response associations (Alvares et al, 2016; Scholl et al, 2022). Thus, the current study suggests that immp2l is not involved in these aspects of ASD or GTS.…”

“…It has been proposed that dysregulation in these neurocircuits may underlie some of the symptoms of ASD and GTS including tics, higher-order repetitive behaviours and compulsive behaviours (Alvares et al, 2016; Delorme et al, 2016; Gillan et al, 2011; Hadjas et al, 2019; Scholl et al, 2022; Singer, 2013). Indeed, both ASD and GTS are characterised by neuroanatomical changes in these circuits post-mortem, including reduced neuron density and numbers of neurons in striatum (Kalanithi et al, 2005; Kataoka et al, 2010; Wegiel et al, 2014) and increased numbers of neurons in prefrontal cortex in ASD (Courchesne et al, 2011; Falcone et al, 2021).…”

“…Thus, well trained instrumental actions in rodents will become less flexible and stimulus driven rather than outcome driven (i.e., mediated by stimulus-response associations), and will therefore be insensitive to changes in outcome value when tested following outcome devaluation in contrast to goal-directed behaviour (Adams, 1982; Dickinson, Balleine, Watt, Gonzalez, & Boakes, 1995). Of particular interest, performance on translational versions of these tasks are altered in individuals with ASD, GTS, OCD, which is suggestive of impaired goal-directed learning due to altered sensitivity to devaluation, or capacity for learning response-outcome or stimulus-response relationships (Alvares, Balleine, Whittle, & Guastella, 2016; Delorme et al, 2016; Gillan et al, 2011; Scholl, Baladron, Vitay, & Hamker, 2022). Further, it has been proposed that tics may resemble habitual behaviour as they are automated, somewhat intentional actions that occur in response to sensory stimuli, and thus may share common neural mechanisms (Delorme et al, 2016; Scholl et al, 2022; Singer, 2013).…”

“…Of particular interest, performance on translational versions of these tasks are altered in individuals with ASD, GTS, OCD, which is suggestive of impaired goal-directed learning due to altered sensitivity to devaluation, or capacity for learning response-outcome or stimulus-response relationships (Alvares, Balleine, Whittle, & Guastella, 2016; Delorme et al, 2016; Gillan et al, 2011; Scholl, Baladron, Vitay, & Hamker, 2022). Further, it has been proposed that tics may resemble habitual behaviour as they are automated, somewhat intentional actions that occur in response to sensory stimuli, and thus may share common neural mechanisms (Delorme et al, 2016; Scholl et al, 2022; Singer, 2013). An imbalance between goal-directed and habit behaviour has also been proposed to underlie inflexible, compulsive and repetitive behaviour, which may be triggered by external stimuli rather than intended goals (Alvares et al, 2016; Gillan et al, 2011; Hadjas, Luscher, & Simmler, 2019).…”