Maturation of prefrontal input to dorsal raphe increases behavioral persistence in mice

The ability to persist towards a desired objective is a fundamental aspect of behavioral control whose impairment is implicated in several behavioral disorders. One of the prominent features of behavioral persistence is that its maturation occurs relatively late in development. This is presumed to echo the developmental time course of a corresponding circuit within late-maturing parts of the brain, such as the prefrontal cortex, but the specific identity of the responsible circuits is unknown. Here, we describe the maturation of the projection from layer 5 neurons of the prefrontal cortex to the dorsal raphe nucleus in mice. We show using pathway-specific optogenetic stimulation that this connection undergoes a dramatic increase in synaptic potency between postnatal weeks 3 and 8, corresponding to the transition from juvenile to adult. We then show that this period corresponds to an increase in the behavioral persistence that mice exhibit in a foraging task. Finally, we use genetic targeting to selectively ablate this pathway in adulthood and show that mice revert to a behavioral phenotype similar to juveniles. These results suggest that the prefrontal to dorsal raphe pathway is a critical anatomical and functional substrate of the development and manifestation of behavioral control.

INFLUENCE OF RAT CENTRAL THALAMIC NEURONS ON FORAGING BEHAVIOR IN A HAZARDOUS ENVIRONMENT

The basolateral amygdala (BL) is a major regulator of foraging behavior. Following BL inactivation, rats become indifferent to predators. However, at odds with the view that the amygdala detects threats and generate defensive behaviors, most BL neurons have reduced firing rates during foraging and at proximity of the predator. In search of the signals determining this unexpected activity pattern, this study considered the contribution of the central medial thalamic nucleus (CMT), which sends a strong projection to BL, mostly targeting its principal neurons. Inactivation of CMT or BL with muscimol abolished the rats’ normally cautious behavior in the foraging task. Moreover, unit recordings revealed that CMT neurons showed large but heterogeneous activity changes during the foraging task, with many neurons decreasing or increasing their discharge rates, with a modest bias for the latter. A generalized linear model revealed that CMT neurons encode many of the same task variables as principal BL cells. However, the nature (inhibitory vs. excitatory) and relative magnitude of the activity modulations seen in CMT neurons differed markedly from those of principal BL cells but were very similar to those of fast-spiking BL interneurons. Together, these findings suggest that, during the foraging task, CMT inputs fire some principal BL neurons, recruiting feedback interneurons in BL, resulting in the widespread inhibition of principal BL cells.

Bayesian approximations to the theory of visual attention (TVA) in a foraging task

Foraging as a natural visual search for multiple targets has increasingly been studied in humans in recent years. Here, we aimed to model the differences in foraging strategies between feature and conjunction foraging tasks found by Kristjánsson et al. (2014). Bundesen (1990) proposed the Theory of Visual Attention (TVA) as a computational model of attentional function that divides the selection process into filtering and pigeonholing. The theory describes a mechanism by which the strength of sensory evidence serves to categorize elements. We combined these ideas to train augmented Naïve Bayesian classifiers using data from Kristjánsson et al. (2014) as input. Specifically, we attempted to answer whether it is possible to predict how frequently observers switch between different target types during consecutive selections (switch rates) during feature and conjunction foraging using Bayesian classifiers. We formulated eleven new parameters that represent key sensory and bias information that could be used for each selection during the foraging task and tested them with multiple Bayesian models. Separate Bayesian networks were trained on feature and conjunction foraging data, and parameters that had no impact on the model's predictability were pruned away. We report high accuracy for switch prediction in both tasks from the classifiers, although the model for conjunction foraging was more accurate. We also report our Bayesian parameters in terms of their theoretical associations to TVA parameters, π_j (denoting the pertinence value) and β_i (denoting the decision-making bias).

Neural encoding of perceived patch value during competitive and hazardous virtual foraging

Natural observations suggest that in safe environments, organisms avoid competition to maximize gain, while in hazardous environments the most effective survival strategy is to congregate with competition to reduce the likelihood of predatory attack. We probed the extent to which survival decisions in humans follow these patterns, and examined the factors that determined individual-level decision-making. In a virtual foraging task containing changing levels of competition in safe and hazardous patches with virtual predators, we demonstrate that human participants inversely select competition avoidant and risk diluting strategies depending on perceived patch value (PPV), a computation dependent on reward, threat, and competition. We formulate a mathematically grounded quantification of PPV in social foraging environments and show using multivariate fMRI analyses that PPV is encoded by mid-cingulate cortex (MCC) and ventromedial prefrontal cortices (vMPFC), regions that integrate action and value signals. Together, these results suggest humans utilize and integrate multidimensional information to adaptively select patches highest in PPV, and that MCC and vMPFC play a role in adapting to both competitive and predatory threats in a virtual foraging setting.

Episodic-like memory is preserved with age in cuttlefish

Episodic memory, remembering past experiences based on unique what–where–when components, declines during ageing in humans, as does episodic-like memory in non-human mammals. By contrast, semantic memory, remembering learnt knowledge without recalling unique what–where–when features, remains relatively intact with advancing age. The age-related decline in episodic memory likely stems from the deteriorating function of the hippocampus in the brain. Whether episodic memory can deteriorate with age in species that lack a hippocampus is unknown. Cuttlefish are molluscs that lack a hippocampus. We test both semantic-like and episodic-like memory in sub-adults and aged-adults nearing senescence ( n = 6 per cohort). In the semantic-like memory task, cuttlefish had to learn that the location of a food resource was dependent on the time of day. Performance, measured as proportion of correct trials, was comparable across age groups. In the episodic-like memory task, cuttlefish had to solve a foraging task by retrieving what–where–when information about a past event with unique spatio-temporal features. In this task, performance was comparable across age groups; however, aged-adults reached the success criterion (8/10 correct choices in consecutive trials) significantly faster than sub-adults. Contrary to other animals, episodic-like memory is preserved in aged cuttlefish, suggesting that memory deterioration is delayed in this species.

Multiplexed action-outcome representation by striatal striosome-matrix compartments detected with a novel cost-benefit foraging task

ABSTRACTLearning about positive and negative outcomes of actions is crucial for survival and underpinned by conserved circuits including the striatum. How associations between actions and outcomes are formed is not fully understood, particularly when the outcomes have mixed positive and negative features. We developed a novel foraging (‘bandit’) task requiring mice to maximize rewards while minimizing punishments. By 2-photon Ca++ imaging, we monitored activity of 5831 identified anterodorsal striatal striosomal and matrix neurons. Surprisingly, we found that action-outcome associations for reward and punishment were combinatorially encoded rather than being integrated as overall outcome value. Single neurons could, for one action, encode outcomes of opposing valence. Striosome compartments consistently exhibited stronger representations of reinforcement outcomes than matrix, especially for high reward or punishment prediction errors. These findings demonstrate a remarkable multiplexing of action-outcome contingencies by single identified striatal neurons and suggest that striosomal neurons are differentially important in action-outcome learning.

Performance-based Social Comparisons in Humans and Long-tailed Macaques

Social comparisons are a fundamental feature of human thinking and affect self-evaluations and task performance. Little is known about the evolutionary origins of social comparison processes, however. Previous studies that investigated performance-based social comparisons in nonhuman primates yielded mixed results. We report three experiments that aimed (a) to explore how the task type may contribute to performance in monkeys, and (b) how a competitive set-up affects monkeys compared to humans. In a co-action touchscreen task, monkeys were neither influenced by nor interested in the performance of the partner. This may indicate that the experimental set-up was not sufficiently relevant to trigger social comparisons. In a novel co-action foraging task, monkeys increased their feeding speed in competitive and co-active conditions, but not in relation to the degree of competition. In an analogue of the foraging task, human participants were affected by partner performance and experimental context, indicating that the task is suitable to elicit social comparisons in humans. Our studies indicate that specifics of task and experimental setting are relevant to draw the monkeys’ attention to a co-actor and that, in line with previous research, a competitive element was crucial. We highlight the need to explore what constitutes “relevant” social comparison situations for monkeys as well as nonhuman animals in general, and point out factors that we think are crucial in this respect (e.g., task type, physical closeness, and the species’ ecology). We discuss that early forms of social comparisons evolved in purely competitive environments with increasing social tolerance and cooperative motivations allowing for more fine-grained processing of social information. Competition driven effects on task performance might constitute the foundation for the more elaborate social comparison processes found in humans, which may involve context-dependent information processing and metacognitive monitoring.

Red Junglefowl Chicks Seek Contact With Humans During Foraging Task

Contact seeking with humans is documented in some domestic animals, mainly dogs, which have advanced communication skills. Domestication as a companion animal is thought to underlie this ability. However, also domesticated horses and goats display similar human-directed behaviors. This suggests either a broader effect of domestication on contact-seeking behavior, or alternatively, that social interactions with humans can result in the development of human contact seeking. As part of another study, we observed contact-seeking behavior in juvenile red junglefowl (Gallus gallus) chicks exposed to behavioral training since hatching, during a foraging task, where chicks were singly required to collect food rewards in a familiar arena using odor cues. If chicks left the arena, we recorded if they approached and looked up at the experimenter, or if they approached other objects (including another human). Chicks approached the experimenter significantly more often than they approached other objects. This behavior was not linked to a fast performance in the test arena, which gave some birds more time to explore the surroundings, or to learning ability measured in a cognitive task. Yet, the preference for the experimenter was lower for chicks that were handled more prior to the experiment. Also, approach probability was positively correlated with escape attempts in a novel arena test. The observed variation in approach behavior suggests a link to aspects of personality, and exposure to human interactions and experimental procedures. Our observations suggest that, although neither domesticated nor selectively bred, red junglefowl that are socialized with humans can potentially develop behavior used to describe contact seeking. Together with evidence from cognitive and behavioral studies, our results suggest that social experiences, not only domestication, can affect human-animal interactions. We propose how interactions between behavior, cognition and handling could be studied further in controlled settings to validate the preliminary findings of our study and uncover the underlying mechanisms.