Can the reward associated with gaze leading train faster gaze shifts to a jointly attended target?

We investigated whether the reward that has previously been associated with initiated joint attention (the experience of having one’s gaze followed by someone else; Pfeiffer et al., 2014, Schilbach et al., 2010) can influence gaze behaviour and, similarly to monetary rewards (Blaukopf & DiGirolamo, 2005; Manohar et al., 2017; Milstein & Dorris, 2007), elicit learning effects. To this end, we adapted Milstein and Dorris (2007) gaze contingent paradigm, so it required participants to look at an anthropomorphic avatar and then conduct a saccade towards the left or right peripheral target. If participants were fast enough, they could experience social reward in terms of the avatar looking at the same target as they did and thus engaging with them in joint attention. One side had higher reward probability than the other (80 % vs 20 %; on the other fast trials the avatar would simply keep staring ahead). We expected that if participants learned about the reward contingency and if they found the experience of having their gaze followed rewarding, their latency and success rate would improve for saccades to the high rewarded targets. Although our current study did not demonstrate that such social reward has a long lasting effect on gaze behaviour, we found that latencies became shorter over time and that latencies were longer on congruent trials (target location was identical to the previous trial) than on noncongruent trials (target location different than on the previous trial), which could reflect inhibition of return.

Rest Is Required to Learn an Appetitively-Reinforced Operant Task in Drosophila

Maladaptive operant conditioning contributes to development of neuropsychiatric disorders. Candidate genes have been identified that contribute to this maladaptive plasticity, but the neural basis of operant conditioning in genetic model organisms remains poorly understood. The fruit fly Drosophila melanogaster is a versatile genetic model organism that readily forms operant associations with punishment stimuli. However, operant conditioning with a food reward has not been demonstrated in flies, limiting the types of neural circuits that can be studied. Here we present the first sucrose-reinforced operant conditioning paradigm for flies. In the paradigm, flies walk along a Y-shaped track with reward locations at the terminus of each hallway. When flies turn in the reinforced direction at the center of the track, they receive a sucrose reward at the end of the hallway. Only flies that rest early in training learn the reward contingency normally. Flies rewarded independently of their behavior do not form a learned association but have the same amount of rest as trained flies, showing that rest is not driven by learning. Optogenetically-induced sleep does not promote learning, indicating that sleep itself is not sufficient for learning the operant task. We validated the sensitivity of this assay to detect the effect of genetic manipulations by testing the classic learning mutant dunce. Dunce flies are learning-impaired in the Y-Track task, indicating a likely role for cAMP in the operant coincidence detector. This novel training paradigm will provide valuable insight into the molecular mechanisms of disease and the link between sleep and learning.

Acetylcholine is released in the basolateral amygdala in response to predictors of reward and enhances the learning of cue-reward contingency

The basolateral amygdala (BLA) is critical for associating initially neutral cues with appetitive and aversive stimuli and receives dense neuromodulatory acetylcholine (ACh) projections. We measured BLA ACh signaling and activity of neurons expressing CaMKIIα (a marker for glutamatergic principal cells) in mice during cue-reward learning using a fluorescent ACh sensor and calcium indicators. We found that ACh levels and nucleus basalis of Meynert (NBM) cholinergic terminal activity in the BLA (NBM-BLA) increased sharply in response to reward-related events and shifted as mice learned the cue-reward contingency. BLA CaMKIIα neuron activity followed reward retrieval and moved to the reward-predictive cue after task acquisition. Optical stimulation of cholinergic NBM-BLA terminal fibers led to a quicker acquisition of the cue-reward contingency. These results indicate BLA ACh signaling carries important information about salient events in cue-reward learning and provides a framework for understanding how ACh signaling contributes to shaping BLA responses to emotional stimuli.

Prospective Representations in Rat Orbitofrontal Ensembles

The orbitofrontal cortex (OFC) has been proposed to encode expected outcomes, which is thought to be important for outcome-directed behavior. However, such neural encoding can also often be explained by the recall of information about the recent past. To dissociate the retrospective and prospective aspects of encoding in the OFC, we designed a non-spatial, continuous, alternating odor-sequence task that mimicked a continuous T-maze. The task consisted of two alternating sequences of four odor-guided trials (2 sequences × 4 positions). In each trial, rats were asked to make a “go” or “no-go” action based on a fixed odor-reward contingency. Odors at both the first and last positions were distinct across the two sequences, such that they resembled unique paths in the past and future, respectively; odors at positions in between were the same and thus resembled a common path. We trained classifiers using neural activity to distinguish between either sequences or positions and asked whether the neural activity patterns in the common path were more like the ones in the past or the future. We found a proximal prospective code for sequence information as well as a distal prospective code for positional information, the latter of which was closely associated with rats’ ability to predict future outcomes. This study demonstrates a prospective behaviorally-relevant predictive code in rat OFC.

Learned Value and Predictiveness affect Gaze but not Figure Assignment

Many factors affect figure-ground segregation, but the contributions of attention and reward history to this process is uncertain. We conducted two experiments to investigate whether reward learning influences figure assignment, and whether this relationship was mediated by attention. Participants learned to associate certain shapes with a reward contingency: during a learning phase, they chose between two shapes on each trial, with subsets of shapes associated with high-probability win, low-probability win, high-probability loss, and low-probability loss. In a test phase, participants were given a figure ground task, in which they indicated which of two regions that shared a contour they perceived as the figure (high probability-win and low-probability win shapes were pitted against each other, as were high probability-loss and low probability-loss shapes). The results revealed that participants had learned the reward contingencies and that, following learning, attention was reliably drawn to the optimal stimulus. Despite this, neither reward history nor the resulting attentional allocation influenced figure-ground organization.

Acetylcholine is released in the basolateral amygdala in response to predictors of reward and enhances learning of cue-reward contingency

The basolateral amygdala (BLA) is critical for associating initially neutral cues with appetitive and aversive stimuli and receives dense neuromodulatory acetylcholine (ACh) projections. We measured BLA ACh signaling and principal neuron activity in mice during cue-reward learning using a fluorescent ACh sensor and calcium indicators. We found that ACh levels and activity of nucleus basalis of Meynert (NBM) cholinergic terminals in the BLA (NBM-BLA) increased sharply in response to reward-related events and shifted as mice learned the tone-reward contingency. BLA principal neuron activity followed reward retrieval and moved to the reward-predictive tone after task acquisition. Optical stimulation of cholinergic NBM-BLA terminal fibers during cue-reward learning led to more rapid learning of the cue-reward contingency. These results indicate that BLA ACh signaling carries important information about salient events in cue-reward learning and provides a framework for understanding how ACh signaling contributes to shaping BLA responses to emotional stimuli.

Balancing Between Goal-Directed and Habitual Responding Following Acute Stress

Instrumental learning is regulated by two memory systems: a relatively rigid but efficient habit system and a flexible but resource-demanding goal-directed system. Previous work has demonstrated that exposure to acute stress may shift the balance between these systems toward the habitual system. In the current study, we used a 2-day outcome devaluation paradigm with a 75% reward contingency rate and altered food reward categories to replicate and extend our previous findings. Participants learned neutral stimulus–response–reward associations on the first day. On the second day, rewards were devalued by eating to satiety. Subsequently, acute stress was induced in half of the participants using the Maastricht Acute Stress Test, while the other half engaged in a nonstressful control task. Finally, relative goal-directed versus habitual behavior was evaluated in a slips-of-action phase, where more slips-of-action indicate a shift toward the habitual system. Results showed that participants successfully acquired the stimulus–response–reward associations, that devaluation was effective, and that stressed participants displayed significant increases in cortisol and blood pressure. Stress led participants to commit more slips-of-action compared with nonstressed controls. The current study extends previous work, showing that the employed paradigm and outcome devaluation procedure are boundary conditions to the stress-induced shift in instrumental responding.

A Clinical Trial Based on Reward Contingency to Improve Prone Tolerance and Motor Development is Feasible in 3- to 6-Month-Old Infants

Aims: The American Academy of Pediatrics recommends “parents to incorporate supervised, awake ‘prone play’ in their infant’s routine to support motor development and minimize the risk of plagiocephaly”. The purpose of this feasibility study was to compare usual care to a reward contingency–based intervention, developed to increase prone tolerance and improve motor skills. Methods: Ten full-term infants, 3–6- months old, with poor prone tolerance were randomized to either the Education group or Reward contingency group. Each group participated in three parent education sessions and 15 intervention sessions, over the period of three weeks. Infants in the Reward contingency group used the Prone Play Activity Center, a technology developed to reinforce motor behavior of infants in prone position. Intervention frequency and parent feedback data determined the feasibility of the interventions. Results: Infants in the Reward contingency group practiced a median of 12 of the 15 anticipated intervention sessions in the Prone Play Activity Center. These infants used the device for a mean of 18 minutes per day. Parents of infants in the Education group practiced a median of 10 sessions of the 15 anticipated intervention sessions. Conclusion: The reward contingency–based intervention is feasible for use in a future clinical trial with some modifications.