Neostriatal Neuronal Activity Correlates Better with Movement Kinematics under Certain Rewards.

Ioan Opris,Randall J Nelson,Mikhail A Lebedev

doi:10.3389/fnins.2016.00336

Abstract

This study investigated how the activity of neostriatal neurons is related to the kinematics of movement when monkeys performed visually and vibratory cued wrist extensions and flexions. Single-unit recordings of 142/236 neostriatal neurons showed pre-movement activity (PMA) in a reaction time task with unpredictable reward. Monkeys were pseudo-randomly (75%) rewarded for correct performance. A regression model was used to determine whether the correlation between neostriatal neuronal activity and the kinematic variables (position, velocity, and acceleration) of wrist movement changes as a function of reward contingency, sensory cues, and movement direction. The coefficients of determination (CoD) representing the proportion of the variance in neuronal activity explained by the regression model on a trial by trial basis, together with their temporal occurrences (time of best regression/correlation, ToC) were compared across sensory modality, movement direction, and reward contingency. The best relationship (correlation) between neuronal activity and movement kinematic variables, given by the average coefficient of determination (CoD), was: (a) greater during trials in which rewards were certain, called “A” trials, as compared with those in which reward was uncertain called (“R”) trials, (b) greater during flexion (Flex) trials as compared with extension (Ext) trials, and (c) greater during visual (VIS) cued trials than during vibratory (VIB) cued trials, for the same type of trial and the same movement direction. These results are consistent with the hypothesis that predictability of reward for correct performance is accompanied by faster linkage between neostriatal PMA and the vigor of wrist movement kinematics. Furthermore, the results provide valuable insights for building an upper-limb neuroprosthesis.

Highlights

IntroductionA significant proportion of neurons from neostriatum (NS) modulate their firing rate in response to environmental stimuli and/or fire before movement initiation and/or execution (Aldridge et al, 1980; Liles, 1985; Schultz and Romo, 1988; Alexander and Crutcher, 1990; Kimura, 1990; Romo and Schultz, 1990; Gardiner and Nelson, 1992; Lebedev and Nelson, 1999; Opris et al, 2011a)
In the present study we recorded the activity of neostriatal neurons in two rhesus monkeys performing wrist movements in a pseudo-random reward task
We examined the relationship between pre-movement activity (PMA) and kinematic variables under three conditions: (a) reward contingency, (b) vibratory vs. visual go-cues, and (c) flexions vs. extensions movements (Opris et al, 2011a)

Summary

Introduction

A significant proportion of neurons from neostriatum (NS) modulate their firing rate in response to environmental stimuli and/or fire before movement initiation and/or execution (Aldridge et al, 1980; Liles, 1985; Schultz and Romo, 1988; Alexander and Crutcher, 1990; Kimura, 1990; Romo and Schultz, 1990; Gardiner and Nelson, 1992; Lebedev and Nelson, 1999; Opris et al, 2011a). Several studies indicate that NS neurons may participate in associating task stimuli with rewards (Schultz and Romo, 1990; Apicella et al, 1991; Robbins and Everitt, 1996; Opris et al, 2009; Schultz, 2010) or in modulating movement vigor (Opris et al, 2011a) This connection between reinforcement and behavior may be mediated by the dopaminergic system at either sub-cortical or cortical levels (Robbins and Everitt, 1996; Schultz et al, 1997). The substantia nigra, ventral striatum and prefrontal cortex may influence segments of the so-called “motor loop” (which includes the dorsal striatum) where pre-movement activity (PMA) often occurs (Alexander et al, 1986; Hoover and Strick, 1993; Graybiel et al, 1994; Watanabe, 1996; Berns et al, 1997)

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