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, 30 (9), 3339-46

Neurons in Anterior Cingulate Cortex Multiplex Information About Reward and Action

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Neurons in Anterior Cingulate Cortex Multiplex Information About Reward and Action

Benjamin Y Hayden et al. J Neurosci.

Abstract

The dorsal anterior cingulate cortex (dACC) is thought to play a critical role in forming associations between rewards and actions. Currently available physiological data, however, remain inconclusive regarding the question of whether dACC neurons carry information linking particular actions to reward or, instead, encode abstract reward information independent of specific actions. Here we show that firing rates of a majority of dACC neurons in a population studied in an eight-option variably rewarded choice task were sensitive to both saccade direction and reward value. Furthermore, the influences of reward and saccade direction on neuronal activity were approximately equal in magnitude over the range of rewards tested and were statistically independent. Our results indicate that dACC neurons multiplex information about both reward and action, endorsing the idea that this area links motivational outcomes to behavior and undermining the notion that its neurons solely contribute to reward processing in the abstract.

Figures

Figure 1.
Figure 1.
Schematic of eight-target saccade choice task and recording location. A, Small yellow fixation point appears, surrounded by eight white squares arranged in a ring. When a monkey fixates on a point, its size shrinks, and after half a second, the monkey is free to shift gaze to one of eight targets. After saccade, all targets change color. Seven (LV targets) turn red, and one (HV target) turns another color. Subsequent saccades have no effect on reward. After a half-second delay, reward is given. B, Between trials, HV target either remains at the same position (60% chance) or moves to an adjacent position (40% chance). Value associated with the HV target is indicated by its color. Only HV trials were analyzed in the present study. C, Recordings were made in the dorsal and ventral banks of the sulcus of the dACC in two monkeys (magnetic resonance image of monkey E shown). Additional details on recording location can be found in the supplemental data (available at www.jneurosci.org as supplemental material). D, Performance of both monkeys on this task. Plot of average likelihood of choosing the optimal target as a function of each possible experienced (gray) and fictive (black) outcomes. For the present study, we focused on HV trials (gray line).
Figure 2.
Figure 2.
Tuning curves for two single neurons from our sample. A, Plot of firing rate of a single neuron on trials with contraversive saccades (dashed gray) and ipsiversive saccades (black). Data are aligned to the onset of the saccade (time 0 on the graph). B, Average firing rate of example dACC neuron during 300 ms epoch after saccades to rewarding targets depends on target position (black lines). Bars indicate 1 SE. Dashed line indicates values for best-fit sine-wave curve. Gray areas represent points that are repeated to emphasize the sinusoidal pattern. C, Firing rate data replotted in polar coordinate system. This neuron fired maximally after saccades to the top right quadrant (contraversive saccades). D, Average firing rate of a different neuron that showed bimodal tuning. E, Firing rate shown in polar coordinate system.
Figure 3.
Figure 3.
Saccade direction tuning in the dACC neuronal population. A, Scatter plot of average firing rate of all neurons in sample versus amplitude of sinusoid fit to their firing rates. Dashed line indicates unity. B, Bar plot of cosine function peak fitted to neuronal tuning functions. Black, Unimodal neurons; white, bimodal neurons. For bimodal neurons, the larger peak is shown. Neurons are more likely to be tuned for contraversive actions (dark gray boxes) than ipsiversive actions (light gray box).
Figure 4.
Figure 4.
Temporal dynamics of saccade direction tuning in dACC neurons. A, Plot of average firing rate of single dACC neuron across critical points in task. Same neuron as in Figure 2. Dashed lines indicate epochs used in analysis. Saccade to target occurs between epochs 4 and 5 (thick dashed line). B, Plot of direction tuning curves for this neuron during each of the epochs analyzed. Bars indicate 1 SE in firing rate. Neuron was weakly tuned for direction during early task epochs, strongly tuned during perisaccadic epochs, and not tuned for saccade direction before and after trials. C, Plot of percentage of neurons showing significant tuning in different task epochs. Horizontal line, Proportion of neurons expected by chance. D, Proportion of neurons exhibiting significant spatial tuning in a direction that differed from the tuning direction observed in the postsaccadic epoch (epoch 5).
Figure 5.
Figure 5.
Saccade direction and reward size are encoded independently by dACC neurons. A, Plot of average firing rate of an example neuron in zero (blue line), low (black line), and high (red line) reward conditions. Although neuron represents both saccade direction and reward size, these two variables are represented independently (i.e., reward does not modulate the gain of the saccade response). B, Plot of effect size for reward (abscissa, response to largest minus response to smallest reward) versus effect size for saccade direction (ordinate, response to peak direction minus response to trough direction). Diagonal line indicates unity.

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