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Reiko Kawagoe

Publications and source records attributed to Reiko Kawagoe.

8 recordsLinked to original sources

Functional differences between macaque prefrontal cortex and caudate nucleus during eye movements with and without reward.

The prefrontal cortex and the basal ganglia form mutually connected networks and are thought to play essential roles together in guiding goal-directed behaviors. Yet, these structures seem to have independent pathways to motor outputs as well, suggesting differential contributions to goal-directed behaviors. We hypothesized that the prefrontal cortex guides actions to a direction required by external demands and the basal ganglia guide actions to an internally motivated direction. To test this hypothesis, we used a task in which monkeys were required to make a memory-guided saccade to a direction indicated by a visual cue while only one direction was associated with reward. We observed a functional dissociation between the lateral prefrontal cortex (LPFC), which commonly represented the cue direction, and the caudate nucleus (CD), which commonly represented the reward-associated direction. Furthermore, cue-directed and reward-directed signals were integrated differently in the two areas; when the cue direction and the reward direction were opposite, LPFC neurons maintained tuning to the cue direction, whereas CD neurons lost the tuning. Different types of spatial tuning in the two brain areas may contribute to different types of goal-directed behavior.

Analysis of Variance↗

A possible role of midbrain dopamine neurons in short- and long-term adaptation of saccades to position-reward mapping.

Dopamine (DA) neurons respond to sensory stimuli that predict reward. To understand how DA neurons acquire such ability, we trained monkeys on a one-direction-rewarded version of memory-guided saccade task (1DR) only when we recorded from single DA neurons. In 1DR, position-reward mapping was changed across blocks of trials. In the early stage of training of 1DR, DA neurons responded to reward delivery; in the later stages, they responded predominantly to the visual cue that predicted reward or no reward (reward predictor) differentially. We found that such a shift of activity from reward to reward predictor also occurred within a block of trials after position-reward mapping was altered. A main effect of long-term training was to accelerate the within-block reward-to-predictor shift of DA neuronal responses. The within-block shift appeared first in the intermediate stage, but was slow, and DA neurons often responded to the cue that indicated reward in the preceding block. In the advanced stage, the reward-to-predictor shift occurred quickly such that the DA neurons' responses to visual cues faithfully matched the current position-reward mapping. Changes in the DA neuronal responses co-varied with the reward-predictive differentiation of saccade latency both in short-term (within-block) and long-term adaptation. DA neurons' response to the fixation point also underwent long-term changes until it occurred predominantly in the first trial within a block. This might trigger a switch between the learned sets. These results suggest that midbrain DA neurons play an essential role in adapting oculomotor behavior to frequent switches in position-reward mapping.

Adaptation, Physiological↗

Dopamine neurons can represent context-dependent prediction error.

Midbrain dopamine (DA) neurons are thought to encode reward prediction error. Reward prediction can be improved if any relevant context is taken into account. We found that monkey DA neurons can encode a context-dependent prediction error. In the first noncontextual task, a light stimulus was randomly followed by reward, with a fixed equal probability. The response of DA neurons was positively correlated with the number of preceding unrewarded trials and could be simulated by a conventional temporal difference (TD) model. In the second contextual task, a reward-indicating light stimulus was presented with the probability that, while fixed overall, was incremented as a function of the number of preceding unrewarded trials. The DA neuronal response then was negatively correlated with this number. This history effect corresponded to the prediction error based on the conditional probability of reward and could be simulated only by implementing the relevant context into the TD model.

Algorithms↗

Reward-predicting activity of dopamine and caudate neurons--a possible mechanism of motivational control of saccadic eye movement.

Recent studies have suggested that the basal ganglia are related to motivational control of behavior. To study how motivational signals modulate motor signals in the basal ganglia, we examined activity of midbrain dopamine (DA) neurons and caudate (CD) projection neurons while monkeys were performing a one-direction-rewarded version (1DR) of memory-guided saccade task. The cue stimulus indicated the goal position for an upcoming saccade and the presence or absence of reward after the trial. Among four monkeys we studied, three were sensitive to reward such that saccade velocity was significantly higher in the rewarded trials than in the nonrewarded trials; one monkey was insensitive to reward. In the reward-sensitive monkeys, both DA and CD neurons responded differentially to reward-indicating and no-reward-indicating cues. Thus DA neurons responded with excitation to a reward-indicating cue and with inhibition to a no-reward-indicating cue. A group of CD neurons responded to the cue in their response fields (mostly contralateral) and the cue response was usually enhanced when it indicated reward. In the reward-insensitive monkey, DA neurons showed no response to the cue, while the cue responses of CD neurons were not modulated by reward. Many CD neurons in the reward-sensitive monkeys, but not the reward-insensitive monkey, showed precue activity. These results suggest that DA neurons, with their connection to CD neurons, modulate the spatially selective signals in CD neurons in the reward-predicting manner and CD neurons in turn modulate saccade parameters with their polysynaptic connections to the oculomotor brain stem.

Animals↗

Correlation of primate caudate neural activity and saccade parameters in reward-oriented behavior.

Changes in the reward context are associated with changes in neuronal activity in the basal ganglia as well as changes in motor outputs. A typical example is found in the caudate (CD) projection neurons and saccade parameters. It raised the possibility that the changes in CD neuronal activity contribute to the changes in saccade parameters. To examine this possibility, we calculated the correlation coefficients (CORs) of the firing rates of each neuron with saccade parameters (peak saccade velocity and latency) on a trial-by-trial basis. We then calculated the mean CORs separately for two CD populations: reward-enhanced type neurons (RENs) that showed enhanced activity and reward-depressed type neurons (RDNs) that showed depressed activity when reward was expected. The activity of RENs was positively correlated with the saccadic peak velocity and negatively correlated with the saccade latency. The activity of RDNs was not significantly correlated with the saccade parameters. We further analyzed the CORs for RENs, a major type of CD neurons. First, we examined the time courses of the CORs using a moving time window (duration: 200 ms). The positive correlation with the saccade velocity and the negative correlation with the saccade latency were present not only in the peri-saccadic period but also during the pre- and postcue periods. Second, we asked whether the CORs with the saccade parameters were direction-selective. A majority of RENs were more active before contralateral saccades (contralateral-preferring neurons) and their activity was correlated more strongly with contralateral saccades than with ipsilateral saccades. A minority of RENs, ipsilateral-preferring neurons, showed no such preference. These results are consistent with the hypothesis that CD neuronal activity exerts facilitatory effects on contralateral saccades and that the effects start well before saccade execution. Furthermore, a multiple regression analysis indicated that changes in activity of some, but not all, CD neurons could be explained by changes in saccade parameters; a major determinant was reward context (presence or absence of reward). These results suggest that, while a majority of CD neurons receive reward-related signals, only some of them can make a significant contribution to change saccadic outputs based on expected reward.

Animals↗

Feature-based anticipation of cues that predict reward in monkey caudate nucleus.

A subset of caudate neurons fires before cues that instruct the monkey what he should do. To test the hypothesis that the anticipatory activity of such neurons depends on the context of stimulus-reward mapping, we examined their activity while the monkeys performed a memory-guided saccade task in which either the position or the color of a cue indicated presence or absence of reward. Some neurons showed anticipatory activity only when a particular position was associated with reward, while others fired selectively for color-reward associations. The functional segregation suggests that caudate neurons participate in feature-based anticipation of visual information that predicts reward. This neuronal code influences the general activity level in response to visual features without improving the quality of visual discrimination.

Animals↗

Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons.

Many neurons show anticipatory activity in learned tasks. This phenomenon appears to reflect the brain's ability to predict future events. However, what actually is predicted is unknown. Using a memory-guided saccade task, in which only one out of four directions was rewarded in each block of trials, we found that a group of neurons in the monkey caudate nucleus (CD) showed activity before presentation of an instruction cue stimulus. Among 329 CD neurons that were related to memory-guided saccade tasks, 156 showed the precue activity and 91 of them were examined fully. Remarkably, the magnitude of the precue activity varied across the four blocks of the one-direction-rewarded (1DR) condition, depending on which direction was rewarded. A majority of neurons with precue activity (83/91, 91%) showed significant directional preference. The best and worst directions were usually in the contralateral and ipsilateral directions, respectively. Within a block, the precue activity increased rapidly for the best direction in 1DR and decreased gradually for the worst direction in 1DR and all-directions-rewarded (ADR) condition. The precue activity was weak in ADR. The precue activity did not reflect the likelihood of a particular cue stimulus, because the probability of the cue appearing in each direction was the same regardless of the rewarded direction. These results suggest that each CD neuron indicates a particular position-reward association prospectively, usually with contralateral preference. Assuming that the CD neurons have access to saccadic motor outputs, the precue activity would create a motivational bias toward the contralateral space, even before an instruction is given by the cue stimulus.

Acoustic Stimulation↗

Modulation of saccadic eye movements by predicted reward outcome.

Reward is a primary goal of behavior and is crucial for survival of animals. To explore the mechanisms underlying such reward-oriented behavior, we devised a memory-guided saccade task in which only one fixed direction out of four was rewarded, which was called the one-direction-rewarded task (1DR). As the rewarded direction was changed in four blocks, saccades in a given direction were rewarded in one block (constituting reward-oriented behavior), but non-rewarded in the other blocks (non-reward-oriented behavior). As a control, an all-directions-rewarded task (ADR) was used. Using these tasks, we found that the parameters of saccades changed depending on whether or not the saccade was followed by reward. (1) The mean saccadic peak velocity was higher and the mean saccade latency was shorter in the rewarded condition than in the non-rewarded condition. (2) The mean saccade amplitude showed no difference in two out of three monkeys. (3) The variations of saccadic velocity, latency and amplitude were smaller in the rewarded condition. (4) Within a block of 1DR, the saccade velocity remained high in the rewarded condition, but decreased gradually in the non-rewarded condition; it decreased only slightly in ADR. The saccade latency showed the opposite pattern of change, but less clearly. (5) The saccades in the non-rewarded condition tended to have slower velocities and longer latencies in the trials shortly after a rewarded trial. (6) The ratio of error trials was much higher in the non-rewarded condition than the rewarded condition. (7) The errors, which were due to premature or incorrect saccades, showed unique spatiotemporal patterns that would reflect the competition between the cognitive and motivational processes. These results provide important constraints to the neuronal mechanism underlying reward-oriented behavior because it must satisfy these rules.

Animals↗