Neuronal activity related to reward size and rewarded target position in primate supplementary eye field

Abstract

Several areas of the macaque brain are known to be related to the reward during the performance of saccadic eye-movement tasks. Neurons in the supplementary eye field (SEF) have been reported to be involved in the prediction and detection of a reward. We describe a group of neurons in the SEF that became active during the period of reward delivery after saccades toward a specific direction, but showed weaker activity in other directions, although the same amount of reward was given in each direction. Moreover, this directional reward activity was modulated by the reward size. Our results demonstrate that the SEF cells may reflect both reward amount and target positions toward which a movement was rewarded, and suggest that they may play an important role in providing information about the value of each saccade according to the spatial target location.

Figure 1.

Recording and stimulation sites (dotted lines) of SEF neurons for monkeys SO and SU. Dotted lines are drawn relative to brain anatomy, constructed from the MRI image. The recordings were centered ∼5 mm to the right or left of the midline for each monkey. Views of the recording and stimulation sites are enlarged. Squares show sites of microstimulation for evoking saccades (threshold ≤50 μA) and recording, circles show sites of recording, and closed symbols indicate the existence of reward-related cells.

Figure 2.

Reward- and saccade-related activity with a directional tuning effect. A, Reward-related activity, shown in raster and histogram format, is aligned to reward onset. The filled dots, filled triangles, and filled squares indicate the Go-signal, Target-in (end of the saccade), and reward onset, respectively. The cell was consistently active during the reward periods after upward saccades and less strongly after left- and right-upward saccades. The center graph indicates the fitted sinusoidal curve of the neuronal activities across eight directions. PD, Preferred direction; r, a correlation coefficient to test the association between the actual firing rate of the reward period and the cosine model prediction. B, Saccade-related activity. The cell was consistently active during the upward saccades and right-up saccade, and less strongly after left-up and rightward saccades. Other conventions are as in A. C, Spatial distribution of the preferred directions of rewarded-target-position-specific activity and saccade-direction-specific activity of SEF cells. Vectors indicate the preferred directions of the reward-related activities (left) or saccade-related activities (right). Three broken circles of different diameters indicate the three levels of significance of correlation between the actual firing rate of the reward (left) or saccade (right) periods and the sine model prediction. D, Comparison between the number of preferred directions contralateral and ipsilateral to recorded SEF. *p < 0.05; **p < 0.01.

Figure 3.

Reward size modulation in SEF cells. The activity in the preferred direction, shown in raster and histogram format, is aligned with reward onset. A, When the monkey received the same amount of reward at the end of each trial through a block (see Materials and Methods), the cell was consistently active during the reward period. B, When small and big rewards were delivered after 16 trials, alternately, through a block (see Materials and Methods), the same cell as in A was consistently active during the big-reward trials. The activity became weaker during the small-reward trials. C, Saccadic eye movements: V, vertical; H, horizontal. Black, Eye-movement traces during the small-reward trials; red, eye movement traces during the big-reward trials. D, E, The neuronal activity of a total of 16 reward-size-related cells are shown on average. Top, Neuronal activity in the preferred direction. Bottom, The neuronal activity in the nonpreferred direction.