Dissecting Motor and Cognitive Component Processes of a Finger-Tapping Task With Hybrid Dopamine Positron Emission Tomography and Functional Magnetic Resonance Imaging.

Filip Grill,Jarkko Johansson,Jan Axelsson,Lars Nyberg,Patrik Brynolfsson,Anna Rieckmann

doi:10.3389/fnhum.2021.733091

Abstract

Striatal dopamine is involved in facilitation of motor action as well as various cognitive and emotional functions. Positron emission tomography (PET) is the primary imaging method used to investigate dopamine function in humans. Previous PET studies have shown striatal dopamine release during simple finger tapping in both the putamen and the caudate. It is likely that dopamine release in the putamen is related to motor processes while dopamine release in the caudate could signal sustained cognitive component processes of the task, but the poor temporal resolution of PET has hindered firm conclusions. In this study we simultaneously collected [11C]Raclopride PET and functional Magnetic Resonance Imaging (fMRI) data while participants performed finger tapping, with fMRI being able to isolate activations related to individual tapping events. The results revealed fMRI-PET overlap in the bilateral putamen, which is consistent with a motor component process. Selective PET responses in the caudate, ventral striatum, and right posterior putamen, were also observed but did not overlap with fMRI responses to tapping events, suggesting that these reflect non-motor component processes of finger tapping. Our findings suggest an interplay between motor and non-motor-related dopamine release during simple finger tapping and illustrate the potential of hybrid PET-fMRI in revealing distinct component processes of cognitive functions.

Highlights

Simple motor tasks like finger tapping have frequently been used to probe the human motor system both in health (Riecker et al, 2003; Turesky et al, 2018) and disease (Elsinger et al, 2003; Wu et al, 2010; Wurster et al, 2015)
In this study we explore DA release patterns during an unrewarded finger tapping task using a novel hybrid PETfMRI imaging approach
DA release in bilateral putamen spatially overlapped with concomitant BOLD response

Summary

Introduction

Simple motor tasks like finger tapping have frequently been used to probe the human motor system both in health (Riecker et al, 2003; Turesky et al, 2018) and disease (Elsinger et al, 2003; Wu et al, 2010; Wurster et al, 2015). Using [11C]Raclopride and the “binding competition” principle, DA release in the bilateral putamen and the caudate during unrewarded finger tapping has been demontrated (Badgaiyan et al, 2003; Goerendt et al, 2003) Both Badgaiyan et al (2003) and Goerendt et al (2003) speculated that DA release in the putamen was reflective of motor demands, consistent with known anatomical projections to the motor cortex, while the caudate responses may have reflected non-motor processes such as learning or attention, which are likely to occur at different timescales than the transient motor specific aspects of the task. Several lines of work indicate a regionally distinctive functional architecture of striatal DA (Haber and Knutson, 2010), but direct evidence for such distinctions in humans has remained elusive This omission primarily pertains to the inherently limited temporal resolution of in vivo PET-techniques (at the timescale of minutes at best), inhibiting the separation between transient motor activity and sustained cognitive component processes

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