Nonequivalent modulation of corticospinal excitability by positive and negative outcomes

Abstract

ObjectiveThe difference between positive and negative outcomes is important in trial‐and‐error decision‐making processes and affects corticospinal excitability. This study investigated corticospinal excitability during the performance of trial‐and‐error decision‐making tasks with varying competing behavioral outcomes.MethodsEach trial began with one of five colored circles presented as a cue. Each color represented a different reward probability, ranging from 10% to 90%. The subjects were instructed to decide whether to perform wrist flexion in response to the cue. Two seconds after the presentation of the cue, a reward stimulus (picture of a coin) or penalty stimulus (mauve circle) was randomly presented to the subject. If the picture of a coin appeared, the subjects received the coin after the experiment if they had performed wrist flexion, but not if they had not performed wrist flexion. If a mauve circle appeared, a coin was deducted from the total reward if the subjects had performed wrist flexion, but not if they had not performed wrist flexion. One second after the reward or penalty stimulus, transcranial magnetic stimulation was delivered to the primary motor cortex at the midpoint between the centers of gravity of the flexor carpi radialis (agonist) and extensor carpi radialis (antagonist) muscles.ResultsCumulative wrist flexions were positively correlated with reward probabilities. Motor evoked potential (MEP) amplitudes in agonist muscles were significantly higher when wrist flexion incurred a penalty than when it incurred a reward, but there was no difference in the MEP amplitudes of antagonist muscles.ConclusionPositive and negative behavioral outcomes differentially altered behavior and corticospinal excitability, and unexpected penalties had a stronger effect on corticospinal excitability for agonist muscles.

Changes in Magnitude and Variability of Corticospinal Excitability During Rewarded Time-Sensitive Behavior

“…This phenomenon termed the “establishing operation” occurs as a result of low reward probability momentarily increasing the value of a consequential reward stimulus (Derosa et al, 2015; Nosik and Carr, 2015; Fisher et al, 2018). In addition, previous studies have suggested that low reward probabilities (Suzuki et al, 2014), upsetting images (Oliveri et al, 2003; Coelho et al, 2010; Borgomaneri et al, 2012), and unexpected penalties also increase corticospinal excitability (Suzuki et al, 2018). These may imply that M1 excitation may increase in line with the “establishing operation” or with no-reward in low reward probability.…”

“…The behavioral experiment was carried out on a different day from the resting state experiment. Previous experiments using reward tasks (Gupta and Aron, 2011; Thabit et al, 2011; Suzuki et al, 2014, 2018) carried out 18–100 trials per condition. Therefore, the time-sensitive reward task comprised three fixed-ratio (FR) schedules of 50 trials per schedule; the 50 trials of the FR A schedule contained a reward stimulus delivered after every response, the 50 trials of the FR B schedule contained a reward stimulus delivered after every two responses, and the 50 trials of the FR C schedule contained a reward stimulus delivered after every four responses.…”

“…In human studies, because the corticospinal tract can be activated by transcranial magnetic stimulation (TMS), it has been suggested that the changes in the magnitude and variability of motor evoked potentials (MEPs) depend on M1 activity (Rösler, 2001). Monetary rewards increase MEP amplitudes for the rewarded behavior (Gupta and Aron, 2011; Kapogiannis et al, 2011; Thabit et al, 2011; Borgomaneri et al, 2014; Pisoni et al, 2014; Suzuki et al, 2014), but deprivation of reward as a penalty also increases MEP amplitudes (Suzuki et al, 2018). These observations suggest that reward probability is functionally related to the effectiveness of a reward stimulus, and reward-related signals modulate M1 motor output and MEPs.…”

“…However, previous studies did not assess the variability of MEP amplitudes but only assessed the magnitude of corticospinal excitability. In addition, previous studies used observational settings without specific behavioral tasks (Kapogiannis et al, 2011; Pisoni et al, 2014) or behavioral tasks unrelated to time perception (Gupta and Aron, 2011; Thabit et al, 2011; Suzuki et al, 2014, 2018). Therefore, it is impossible to know whether expecting a reward or non-reward, based on reward probability, affects the magnitude and variability of corticospinal excitability during time-sensitive behavioral tasks and whether the observed reward-related corticospinal excitability changes are associated with time-sensitive behavioral changes.…”

Reward modulates behaviour and neural responses in motor cortex during action observation

“…Several studies observed that M1 excitability is modulated by direct rewards or by reward expectation during motor tasks (Bundt, Abrahamse, Braem, Brass, & Notebaert, 2016;Gupta & Aron, 2011;Kapogiannis et al, 2008;Klein-Flugge & Bestmann, 2012;Mooshagian, Keisler, Zimmermann, Schweickert, & Wassermann, 2015;Suzuki, Hamaguchi, & Matsunaga, 2018;Suzuki et al, 2014;Thabit et al, 2011). It is also clear from the literature that many brain areas involved in reward processing, such as striatum, ventral tegmental area (VTA), anterior cingulate cortex (ACC), supplementary motor area (SMA), orbitofrontal cortex and amygdala, are influencing premotor and motor cortices (Campos, 2005;FitzGerald, Friston, & Dolan, 2012;Gottfried, O'Doherty, & Dolan, 2003;Hosp, Pekanovic, Rioult-Pedotti, & Luft, 2011;Kunori, Kajiwara, & Ichiro Takashima, 2014;Leemburg, Canonica, & Luft, 2018;Schultz, 2000;Wickens, Reynolds, & Hyland, 2003;Williams, Bush, Rauch, Cosgrove, & Eskandar, 2004).…”