Research Article: Motor Cortex-Evoked Activity in Reciprocal Muscles Is Modulated by Reward Probability

Date Published: March 6, 2014

Publisher: Public Library of Science

Author(s): Makoto Suzuki, Hikari Kirimoto, Kazuhiro Sugawara, Mineo Oyama, Sumio Yamada, Jun-ichi Yamamoto, Atsuhiko Matsunaga, Michinari Fukuda, Hideaki Onishi, Berthold Langguth.


Horizontal intracortical projections for agonist and antagonist muscles exist in the primary motor cortex (M1), and reward may induce a reinforcement of transmission efficiency of intracortical circuits. We investigated reward-induced change in M1 excitability for agonist and antagonist muscles. Participants were 8 healthy volunteers. Probabilistic reward tasks comprised 3 conditions of 30 trials each: 30 trials contained 10% reward, 30 trials contained 50% reward, and 30 trials contained 90% reward. Each trial began with a cue (red fixation cross), followed by blue circle for 1 s. The subjects were instructed to perform wrist flexion and press a button with the dorsal aspect of middle finger phalanx as quickly as possible in response to disappearance of the blue circle without looking at their hand or the button. Two seconds after the button press, reward/non-reward stimulus was randomly presented for 2-s duration. The reward stimulus was a picture of Japanese 10-yen coin, and each subject received monetary reward at the end of experiment. Subjects were not informed of the reward probabilities. We delivered transcranial magnetic stimulation of the left M1 at the midpoint between center of gravities of agonist flexor carpi radialis (FCR) and antagonist extensor carpi radialis (ECR) muscles at 2 s after the red fixation cross and 1 s after the reward/non-reward stimuli. Relative motor evoked potential (MEP) amplitudes at 2 s after the red fixation cross were significantly higher for 10% reward probability than for 90% reward probability, whereas relative MEP amplitudes at 1 s after reward/non-reward stimuli were significantly higher for 90% reward probability than for 10% and 50% reward probabilities. These results implied that reward could affect the horizontal intracortical projections in M1 for agonist and antagonist muscles, and M1 excitability including the reward-related circuit before and after reward stimulus could be differently altered by reward probability.

Partial Text

Reward plays an important role in motor learning [1] and in the induction of synaptic plasticity [2]–[6]. In mammals, dopaminergic (DA) neurons in the ventral tegmental area of the substantia nigra respond with increases and decreases in their firing rate as a consequence of rewarding stimuli [7]. Among the areas potentially influencing the primary motor cortex (M1), many are involved in reward processing, including the substantia nigra and striatum [1], [8]–[12]. Recent retrograde tracing research found about 70% of DA midbrain neurons projecting to M1 were located in the ventral tegmental area [13]. In M1, DA terminals are distributed inhomogeneously with a preference for deep cortical layers V and VI [14]. Regarding postsynaptic elements, D1 and D2 receptors are expressed in both superficial (I, II, and III) and deep (V and VI) layers [15]. In addition, animal experimentation has suggested that extensive, horizontally oriented, intrinsic axon collaterals in layers III and V provide inputs to many different movement representations in M1 [16]. In human experimentation, the output from the common M1 site may diverge onto agonist and antagonist muscles with different “gain” according to the final movement to be performed, presumably regulated by the horizontal intracortical projections interconnecting functionally related neuronal clusters within M1 [17]. DA neurons may play a significant role in this context. Recent studies [14] revealed that dopamine modulates M1 circuitry by affecting various processes of motor learning-dependent plasticity. Motor skill learning induces a long-lasting increase in synaptic strength in M1 horizontal connections of layers II/III suggesting an association with long-term potentiation (LTP)-like plasticity [18], [19]. The D1-receptor antagonist SCH29339 and the D2-receptor antagonist raclopride markedly reduced the ability of M1 horizontal connections to form LTP [6]. These results would suggest that intact DA signaling is necessary for synaptic plasticity in M1 and reward information may influence motor behavior by modulating the excitability of the M1 to diverge onto agonist and antagonist muscles.

All subjects completed all experimental conditions. None of the subjects experienced any side effects from TMS during the experiments.

In the present study, we observed a change in M1 excitability for reciprocal muscles during the performance of probabilistic reward tasks. The results of this study indicated that (a) relative MEP amplitudes of agonist (FCR) and antagonist (ECR) muscles before reward stimulus were highest for 10% reward probability during probabilistic reward tasks, (b) relative MEP amplitudes of agonist and antagonist muscles after reward stimulus presentation were highest for 90% reward probability during probabilistic reward tasks, (c) relative MEP amplitudes of agonist and antagonist muscles after non-reward stimulus presentation were not changed during probabilistic reward tasks, and (d) SICI of the agonist muscle was decreased after 10% probabilistic reward tasks. These systematic observations provided evidence that M1 excitability for reciprocal muscles was affected by reward probability. To our knowledge, this is the first systematic study to demonstrate a change in M1 excitability for reciprocal muscles during the performance of probabilistic reward tasks.