Tourette syndrome: a disorder of the social decision-making network

Abstract

Tourette syndrome is a common neurodevelopmental disorder defined by characteristic involuntary movements, tics, with both motor and phonic components. Tourette syndrome is usually conceptualized as a basal ganglia disorder, with an emphasis on striatal dysfunction. While considerable evidence is consistent with these concepts, imaging data suggest diffuse functional and structural abnormalities in Tourette syndrome brain. Tourette syndrome exhibits features that are difficult to explain solely based on basal ganglia circuit dysfunctions. These features include the natural history of tic expression, with typical onset of tics around ages 5 to 7 years and exacerbation during the peri-pubertal years, marked sex disparity with higher male prevalence, and the characteristic distribution of tics. The latter are usually repetitive, somewhat stereotyped involuntary eye, facial and head movements, and phonations. A major functional role of eye, face, and head movements is social signalling. Prior work in social neuroscience identified a phylogenetically conserved network of sexually dimorphic subcortical nuclei, the Social Behaviour Network, mediating many social behaviours. Social behaviour network function is modulated developmentally by gonadal steroids and social behaviour network outputs are stereotyped sex and species specific behaviours. In 2011 O'Connell and Hofmann proposed that the social behaviour network interdigitates with the basal ganglia to form a greater network, the social decision-making network. The social decision-making network may have two functionally complementary limbs: the basal ganglia component responsible for evaluation of socially relevant stimuli and actions with the social behaviour network component responsible for the performance of social acts. Social decision-making network dysfunction can explain major features of the neurobiology of Tourette syndrome. Tourette syndrome may be a disorder of social communication resulting from developmental abnormalities at several levels of the social decision-making network. The social decision-making network dysfunction hypothesis suggests new avenues for research in Tourette syndrome and new potential therapeutic targets.

Keywords: basal ganglia; brain development; habit-based behaviour; neuroendocrine system; tic disorder.

Figure 1

The Social Behaviour Network (SBN). Adapted from Newman (1999). This network mediates a large number of relatively stereotyped social behaviours, is modulated by gonadal steroids, and has sex dimorphic components. The PAG is the main efferent node, driving lower circuits responsible for specific behaviours. AH = anterior hypothalamus; MA = medial amgydala; LS = lateral septum.

Figure 2

The Social Decision-making Network (SDM). Reprinted with permission from O’Connell and Hofmann (2011). This network combines crucial basal ganglia circuits with the SBN to form a greater network mediating evaluation of social signals, selection of appropriate social behaviours, and the initiation of relevant social behaviours. This cartoon omits direct projections from SBN hypothalamic nuclei to the VTA. AH = anterior hypothalamus; blAMY = basolateral amygdala; HIP = hippocampal formation; LS = lateral septum; meAMY = medial amygdala; NAcc = nucleus accumbens; PAG/CG = periaqueductal grey/central grey; POA = medial preoptic area; Str = striatum; VP = ventral pallidum.

Figure 3

Two limb model of the SDM for maternal, and male and female sexual behaviours. Projections from VMH and MPOA to PAG are responsible for consummatory behaviours. projections from the MPOA to the VTA, with subsequent dopaminergic signalling in the ventral striatum, are responsible for appetitive behaviours, including evaluation of the motivational significance of stimuli. Adapted from Stolzenberg and Numan (2011).