scholarly journals Encoding of reward expectation by monkey anterior insular neurons

2012 ◽  
Vol 107 (11) ◽  
pp. 2996-3007 ◽  
Author(s):  
Takashi Mizuhiki ◽  
Barry J. Richmond ◽  
Munetaka Shidara

The insula, a cortical brain region that is known to encode information about autonomic, visceral, and olfactory functions, has recently been shown to encode information during reward-seeking tasks in both single neuronal recording and functional magnetic resonance imaging studies. To examine the reward-related activation, we recorded from 170 single neurons in anterior insula of 2 monkeys during a multitrial reward schedule task, where the monkeys had to complete a schedule of 1, 2, 3, or 4 trials to earn a reward. In one block of trials a visual cue indicated whether a reward would or would not be delivered in the current trial after the monkey successfully detected that a red spot turned green, and in other blocks the visual cue was random with respect to reward delivery. Over one-quarter of 131 responsive neurons were activated when the current trial would (certain or uncertain) be rewarded if performed correctly. These same neurons failed to respond in trials that were certain, as indicated by the cue, to be unrewarded. Another group of neurons responded when the reward was delivered, similar to results reported previously. The dynamics of population activity in anterior insula also showed strong signals related to knowing when a reward is coming. The most parsimonious explanation is that this activity codes for a type of expected outcome, where the expectation encompasses both certain and uncertain rewards.

2021 ◽  
Author(s):  
Sa-Ik Hong ◽  
Seungwoo Kang ◽  
Minryung Song ◽  
Minsu Yang ◽  
Matthew Baker ◽  
...  

Abstract The external globus pallidus (GPe) is an integrative hub and gateway for behavioral flexibility in reward-related behaviors. However, it remains unknown whether enriched astrocytes in the GPe guide behavioral flexibility. Here, we trained mice to exhibit goal-directed and habitual reward-seeking behaviors using the behavior tasks with effort- and time-based reward delivery, respectively. Then, we examined the temporal dynamics of GPe astrocytes during goal-directed and habitual learning. Overall, GPe astrocytes were substantially silenced during habitual learning compared to goal-directed learning. In the timescale of action events, GPe astrocyte activities were increased immediately after termination of reward-taking behavior before the following action. However, during habitual learning, the increase of astrocyte activity was not evident. Moreover, support vector machine (SVM) analysis demonstrated that GPe astrocytes dynamics predicted whether mice perform goal-directed or habitual behaviors. Interestingly, chemogenetic activation of GPe astrocytes, which dampened GPe neuronal firings and habitual behaviors, exhibting goal-directed behaviors. Strikingly, brief and repeated attentional stimulations recapitulated the effect of chemogenetic activation of GPe in intervening the habitual reward-seeking behaviors with increased GPe astrocyte activities. Our findings reveal a novel insight that increasing GPe astrocytic activities attenuates habitual behavior and improves behavioral flexibility, which may provide a potential therapeutic target for decision-making-related disorders, such as obsessive-compulsive disorder and addiction.


2021 ◽  
Author(s):  
Przemyslaw Jarzebowski ◽  
Y. Audrey Hay ◽  
Benjamin F. Grewe ◽  
Ole Paulsen

SummaryHippocampal neurons encode a cognitive map for spatial navigation1. When they fire at specific locations in the environment, they are known as place cells2. In the dorsal hippocampus place cells accumulate at current navigational goals, such as learned reward locations3–6. In the intermediate-to-ventral hippocampus (here collectively referred to as ventral hippocampus), neurons fire across larger place fields7–10 and regulate reward- seeking behavior11–16, but little is known about their involvement in reward-directed navigation. Here, we compared the encoding of learned reward locations in the dorsal and ventral hippocampus during spatial navigation. We used calcium imaging with a head- mounted microscope to track the activity of CA1 cells over multiple days during which mice learned different reward locations. In dorsal CA1 (dCA1), the overall number of active place cells increased in anticipation of reward but the recruited cells changed with the reward location. In ventral CA1 (vCA1), the activity of the same cells anticipated the reward locations. Our results support a model in which the dCA1 cognitive map incorporates a changing population of cells to encode reward proximity through increased population activity, while the vCA1 provides a reward-predictive code in the activity of a specific subpopulation of cells. Both of these location-invariant codes persisted over time, and together they provide a dual hippocampal reward-location code, assisting goal- directed navigation17, 18.


2006 ◽  
Vol 18 (2) ◽  
pp. 212-226 ◽  
Author(s):  
Satoe Ichihara-Takeda ◽  
Shintaro Funahashi

Reward-period activity observed in the dorsolateral prefrontal cortex (DLPFC) and the orbitofrontal cortex (OFC) is thought to represent the detection of reward delivery. To investigate whether this activity plays the same role in these areas, we examined this activity under different reward schedules and whether the reward schedule has similar effects on this activity in each of these areas. A monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, the monkey received a large amount of reward only after four successful trials, whereas in the ODR-2 schedule, it received a small amount of reward after every successful trial. Although reward-period activity was observed in both areas, more neurons exhibited this activity in the OFC. Reward-period activity was modulated by the proximity to reward delivery in both areas and this feature was observed more frequently in the OFC. The onset time of this activity also gradually advanced depending on the proximity to reward delivery. Moreover, many OFC neurons with this activity responded to free reward delivery. These results indicate that reward-period activity in the OFC represents the detection of reward delivery and that the gradual change in the magnitude and the onset time of this activity represents the expectation of reward delivery. Similar features of reward-period activity were observed in DLPFC neurons, although a significant number of DLPFC neurons did not respond to free reward delivery and no advance was observed in the onset time of this activity. These results suggest that reward-period activity in the DLPFC participates in whether or not correct performance was achieved. Thus, although similar reward-period activity was observed in both areas, the activity in the OFC represents the detection of reward delivery and is affected by the monkey's motivational state, whereas that in the DLPFC seems to participate in monitoring whether or not the necessary performance is achieved.


2010 ◽  
Vol 68 ◽  
pp. e287
Author(s):  
Tsuyoshi Setogawa ◽  
Takashi Mizuhiki ◽  
Kiyonori Inaba ◽  
Munetaka Shidara

2020 ◽  
Author(s):  
Elizabeth Hanson ◽  
Katie L Brandel-Ankrapp ◽  
Benjamin R Arenkiel

AbstractSensory perception underlies how we internalize and interact with the external world. In order to adapt to changing circumstances and interpret signals in a variety of contexts, sensation needs to be reliable, but perception of sensory input needs to be flexible. An important mediator of this flexibility is top-down regulation from the cholinergic basal forebrain. Basal forebrain projection neurons serve as pacemakers and gatekeepers for downstream neural networks, modulating circuit activity across diverse neuronal populations. This top-down control is necessary for sensory cue detection, learning, and memory, and is disproportionately disrupted in neurodegenerative diseases associated with cognitive decline. Intriguingly, cholinergic signaling acts locally within the basal forebrain to sculpt the activity of basal forebrain output neurons. To determine how local cholinergic signaling impacts basal forebrain output pathways that participate in top-down regulation, we sought to define the dynamics of cholinergic signaling within the basal forebrain during motivated behavior and learning. Towards this, we utilized fiber photometry and the genetically encoded acetylcholine indicator GAChR2.0 to define temporal patterns of cholinergic signaling in the basal forebrain during olfactory-guided, motivated behaviors and learning. We show that cholinergic signaling reliably increased during reward-seeking behaviors but was strongly suppressed by reward delivery in a go/no-go, olfactory-cued discrimination task. The observed transient reduction in cholinergic tone was mirrored by a suppression in basal forebrain GABAergic neuronal activity. Together, these findings suggest that cholinergic tone in the basal forebrain changes rapidly to reflect rewardseeking behavior and positive reinforcement to impact basal forebrain circuit activity.


2008 ◽  
Vol 20 (4) ◽  
pp. 563-579 ◽  
Author(s):  
Satoe Ichihara-Takeda ◽  
Shintaro Funahashi

Recent studies show that task-related activity in the dorsolateral prefrontal cortex (DLPFC) is modulated by the quality and quantity of the reward, suggesting that the subject's motivational state affects cognitive operations in the DLPFC. The orbito-frontal cortex (OFC) is a possible source of motivational inputs to the DLPFC. However, it is not well known whether these two areas exhibit similar motivational effects on task-related activity. We compared motivational effects on task-related activity in these areas while a monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, reward was given only after the successful completion of four consecutive trials, whereas in the ODR-2 schedule, reward was given after every correct trial. Task-related activities in both areas showed spatial selectivity. The spatial characteristics of task-related activity remained constant in both schedules. Task-related activity in both areas, especially delay-period activity, was also affected by the reward schedule and the magnitude of the activity gradually increased depending on the proximity of the reward trial in the ODR-1 schedule. More task-related OFC activities were affected by reward schedules, whereas more task-related DLPFC activities were affected by spatial factors and reward schedules. These results indicate that the OFC plays a role in monitoring the proximity of the reward trial and detecting reward delivery, whereas the DLPFC plays a role in performing cognitive operations and integrating cognitive and motivational information. These results also indicate that spatial information and the animal's motivational state independently affect neuronal activity in both areas.


2021 ◽  
Author(s):  
Andrew T Marshall ◽  
Sean B. Ostlund

The Pavlovian-instrumental transfer (PIT) paradigm is widely used to assay the motivational influence of reward-paired cues, which is reflected by their ability to stimulate instrumental reward-seeking behavior. Leading models of incentive learning assume that motivational value is assigned to cues based on the total amount of reward they signal (i.e., their state value). Based on recent findings, we lay out the alternative hypothesis that cue-elicited reward predictions may actually suppress the motivation to seek out new rewards through instrumental behavior in order to facilitate efficient retrieval of a reward that is already expected, before it is lost or stolen. According to this view, cue-motivated reward seeking should be inversely related to the magnitude of an expected reward, since there is more to lose by failing to secure a large reward than a small reward. We investigated the influence of expected reward magnitude on PIT expression. Hungry rats were initially trained to lever press for food pellets before undergoing Pavlovian conditioning, in which two distinct auditory cues signaled food pellet delivery at cue offset. Reward magnitude was varied across cues and groups. While all groups had at least one cue that signaled three food pellets, the alternate cue signaled either one (Group 1/3), three (Group 3/3), or nine food pellets (Group 3/9). PIT testing revealed that the motivational influence of reward-predictive cues on lever pressing varied inversely with expected reward magnitude, with the 1-pellet cue augmenting performance and the 3- and 9-pellet cues suppressing performance, particularly near the expected time of reward delivery. This pattern was mirrored by opposing changes in the food-port entry behavior, which varied positively with expected reward magnitude. We discuss how these findings may relate to cognitive control over cue-motivated behavior.


2009 ◽  
Vol 65 ◽  
pp. S190
Author(s):  
Kiyonori Inaba ◽  
Takashi Mizuhiki ◽  
Koji Toda ◽  
Shigeru Ozaki ◽  
Kanako Yaguchi ◽  
...  

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