Speech-induced striatal dopamine release is left lateralized and coupled to functional striatal circuits in healthy humans: A combined PET, fMRI and DTI study

Abstract

Considerable progress has been recently made in understanding the brain mechanisms underlying speech and language control. However, the neurochemical underpinnings of normal speech production remain largely unknown. We investigated the extent of striatal endogenous dopamine release and its influences on the organization of functional striatal speech networks during production of meaningful English sentences using a combination of positron emission tomography (PET) with the dopamine D2/D3 receptor radioligand [11C]raclopride and functional MRI (fMRI). In addition, we used diffusion tensor tractography (DTI) to examine the extent of dopaminergic modulatory influences on striatal structural network organization. We found that, during sentence production, endogenous dopamine was released in the ventromedial portion of the dorsal striatum, in its both associative and sensorimotor functional divisions. In the associative striatum, speech-induced dopamine release established a significant relationship with neural activity and influenced the left-hemispheric lateralization of striatal functional networks. In contrast, there were no significant effects of endogenous dopamine release on the lateralization of striatal structural networks. Our data provide the first evidence for endogenous dopamine release in the dorsal striatum during normal speaking and point to the possible mechanisms behind the modulatory influences of dopamine on the organization of functional brain circuits controlling normal human speech.

Abnormal Striatal Dopaminergic Neurotransmission during Rest and Task Production in Spasmodic Dysphonia

“…This may be explained by the fact that spasmodic dysphonia symptoms typically plateau within the first year after the onset and remain unchanged for life in the majority of patients, while only a subset of patients reports worsening or improvement of their symptoms over time (Izdebski et al, 1984;Aronson, 1990;Tanner et al, 2011). In this study, all patients with spasmodic dysphonia had stable symptoms for at least 6 years, and none reported significant progression of their voice symptoms.…”

“…This may be associated with altered dopamine release during task production. Based on our previous findings of abnormal functional activity during both symptomatic and asymptomatic tasks in spasmodic dysphonia (Simonyan and Ludlow, 2010), we expected to identify changes in RAC ⌬BP during both symptomatic speaking and asymptomatic finger tapping. We hypothesized that some of these abnormalities may be linked to clinical and subclinical features of spasmodic dysphonia, possibly contributing to the manifestation of this disorder.…”

Altered resting‐state functional connectivity of the putamen and internal globus pallidus is related to speech impairment in Parkinson's disease

“…This finding is consistent with a study by Simonyan et al. (2013) who found that BOLD activity in the left anterior putamen was positively correlated with activity in left STG during sentence production. The results of these comparisons suggest that, while PDSI subjects have widespread reductions in connectivity between the left putamen and cerebral cortex (including cortical areas involved in speech production), reduced functional connectivity between the putamen and left STG may be uniquely linked to speech impairments in PD.…”

“…Given that striatal dopamine release appears to be left‐lateralized during speech production (Simonyan et al. 2013), we further predicted that striatal connectivity differences between PDN and PDSI groups would occur in the left striatum. Although several speech models include the globus pallidus, none are predictive of whether there are resting‐state connectivity changes related to speech impairment in PD.…”

“…Researchers have reported increased bilateral putamen activation during both speech and nonspeech vocal tract movements using fMRI (Brown et al., 2009; Chang, Kenney, Loucks, Poletto, & Ludlow, 2009; Parkinson et al., 2012). A recent PET study using D2/D3 receptor radioligands also demonstrated that speech production is accompanied by a left‐lateralized increase in endogenous dopamine release within the striatum (Simonyan, Herscovitch, & Horwitz, 2013), suggesting that left‐hemisphere striatal regions may in fact play a more important role than those in the right hemisphere. In addition to the striatum, the role of the pallidum has also been described in relation to normal speech production.…”