Role for cingulate motor area cells in voluntary movement selection based on reward

Science

Volumn 282, Issue 5392, 1998, Pages 1335-1338

  Shima, Keisetsu ^a   Tanji, Jun ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CINGULATE GYRUS; INFORMATION PROCESSING; MONKEY; MOTONEURON; MOTOR ACTIVITY; NONHUMAN; PRIORITY JOURNAL; REWARD; VOLUNTARY MOVEMENT;

EID: 0032515019     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.282.5392.1335     Document Type: Article

References (33)

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12. The animals were cared for in accordance with NIH's Guide for Care and Use of Laboratory Animals, and Guidelines for Institutional Animal Care and Use published by Tohoku University School of Medicine.
13. Behavioral task: When the monkey held the handle in a neutral position for 2.8 to 7.8 s, an LED (light-emitting diode) was illuminated as a signal to start the correct movement. Initially, the subject had to guess which of the two choices was correct. Performing the correct movement was rewarded with a drop of fruit juice, and the correct movement remained unchanged in a block of trials, so that the monkey was required to keep selecting the same movement. The amount of the reward remained constant (0.1 ml) for four to 12 successive trials, unless the subject made a mistake and selected the wrong movement, in which case an audible warning tone replaced the reward. Subsequently, the amount of the reward decreased by 30% for each correct trial. At this stage, monkeys were free to select the alternate movement. They usually did so after the first to the third decrement (30 to 65.7% decrease in reward). If they did, the alternate movement was then defined as the correct movement, the reward reverted to the full amount, and a new series of constant-reward trials began, with the redefined correct movement.
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16. After completion of recording cellular activity, recording sites were marked with microlesions (by passing small currents through recording electrodes). Thereafter, the primary motor cortex was carefully mapped with intracortical microstimulation. A chemical tracer, wheat-germ agglutinin-horseradish peroxidase (WGA-HRP, 0.2 μl), was injected into four sites within both the proximal and distal forelimb areas of the primary motor cortex. In the recording sites in the CMAs, HRP-positive cells were found with a standard technique (10). Because we found no spread of injected WCA-HRP into the face area, we concluded that the portions of CMAr and CMAc from where we recorded cellular activity coincided with the areas that projected to arm representation areas of the primary motor cortex.
17. Intracortical microstimulation was delivered with 20 to 40 pulses of 0.2-ms duration at 333 Hz at 20 to 50 μA. Responses of cells to somatosensory stimulation (responses to joint manipulations or stroking the skin) also helped to find that the recording sites were forelimb representation areas and not face or neck areas.
18. Neuronal activity was quantitatively analyzed after constructing a peri-event histogram by summing the data from at least 10 trials for each condition. We defined the activity as task-related when the number of discharges in at least three successive 20-ms bins of the peri-event histogram during the four task periods deviated from the mean value during a control period by more than 2 SDs. The task periods included preparatory (from the time the handle was held in the central position to the trigger signal), premovement (from the trigger signal to the onset of movement), postmovement (from the onset of movement to delivery of the reward, 400 ms after the execution of the movement), and reward (500 ms after reward delivery). The control period was the last 500 ms of the intertrial interval. We performed analysis of variance (ANOVA) to test whether the activity in the reduced reward condition differed from that in the ordinary reward condition for the data obtained on a trial-by-trial basis.
19. We performed ANOVA to test this difference.
20. This finding suggests that the activity of these selective cells influences a motor decision process (facilitating selection of one movement and suppressing the other), rather than reflecting an affective aspect of the reward.
21. Y. Matsuzaka and J. Tanji, J. Neurophysiol. 76, 2327 (1996).
22. The neurons were recorded from both the proximal (arm) and distal (hand) representation areas in the primary motor cortex, defined by the effects of intracortical microstimulation. In addition to this study on the 114 neurons in these areas, we also examined neuronal responses in the neck, back, and shoulder representation areas. In these areas, we did not observe the selective responses appearing after the reduced reward. We also analyzed extensively the activity in the neck and back muscles (with electromyogram) and found no responses appearing selectively after the reduced reward.
23. After completing the cellular recording sessions, we inserted small-caliber (300 μm) injection cannulae bilaterally into the CMAs and injected a small amount (2 to 4 μl, 1 to 10 μg/μl, 1 μl in 10 min) of muscimol to evaluate the effects of temporary deactivation of each area. The least effective concentration was 5 μg/μl.
24. The reaction time (defined as the interval between the beginning of the "start" signal and the movement onset) and movement time (the interval from the movement onset to the attainment of the required motor-target) during performance of the motor task were always analyzed. When the movement alteration was cued with the tone signal, neither values was found to be significantly different when compared before and after the muscimol injection (P > 0.1 by Mann-Whitney U test). This means that the animals' ability to execute the movements per se was not much influenced by the muscimol application. However, after the muscimol injection, the reaction time was lengthened (P < 0.01) when the animal selected the alternate movement in response to the reduced reward, although the movement time was not lengthened (P > 0.05).
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33. Supported by a Grant-in-Aid for Scientific Research on Priority Areas from the Japanese Ministry of Education, Science, Sports and Culture.