Anticipatory dynamics in the human brain guide foraging for primary rewards

Foraging is a fundamental food-seeking behavior in a wide range of species that enables survival in an uncertain world. During foraging, behavioral agents constantly face a trade-off between staying in their current location or exploring another. Despite ethological generality and importance of foraging, it remains unclear how the human brain guides continuous decision in such situations. Here we show that anticipatory activity dynamics in the anterior prefrontal cortex (aPFC) and hippocampus underpin foraging for primary rewards. While functional MRI was performed, humans foraged for real liquid rewards available after tens of seconds, and continuous decision during foraging was tracked by a dynamic pattern of brain activity that reflected anticipation of a future reward. When the dynamic anticipatory activity in the aPFC was enhanced, humans remained in their current environment, but when this activity diminished, they explored a new environment. Moreover, the anticipatory activity in the aPFC and hippocampus was associated with distinct decision strategies: aPFC activity was enhanced in humans adopting an exploratory strategy, whereas those remaining stationary showed enhanced activity in the hippocampus. Our results suggest that anticipatory dynamics in the fronto-hippocampal mechanisms underlie continuous decision-making during human foraging.

Chronic caffeine treatment disrupts the circadian rhythm in Drosophila

The circadian clock governs the timing of sleep-wake cycles as well as of other behavioural, physiological and metabolic processes. While the endogenous circadian clock mediates the timing of sleep, homeostatic mechanisms modulate the amount and depth of sleep. Evidence from previous studies showed that caffeine intake promotes wakefulness, whereas adult-stage specific caffeine treatment not only suppresses sleep but also delays the phase of circadian rhythm in Drosophila. In humans, caffeine is consumed on a daily basis and hence it is important to understand the effect of prolonged caffeine intake on circadian and homeostatic regulation of sleep. In the present study we examined the differential effect of acute and chronic caffeine treatment on sleep ontogeny as well as on circadian and homeostatic regulation of sleep in Drosophila. The results of our study showed that acute caffeine treatment reduces day and night sleep in mature flies through the homeostatic pathway whereas it reduced only the day sleep in young flies. Chronic caffeine treatment did not exert any significant effect on sleep in young flies. On the other hand, it delayed the timing of sleep in mature flies and in addition flies under higher caffeine concentration reduced the morning and evening anticipatory activity under 12 hour: 12 hour light: dark cycles. These flies also exhibited either a longer free running period or arrhythmicity under constant darkness. The results of our study showed that acute caffeine treatment suppresses sleep through the homeostatic pathway whereas prolonged caffeine treatment disrupts the circadian rhythm in mature flies.

Oxytocinergic cells of the posterior hypothalamic paraventricular nucleus participate in the food entrained clock

The mechanisms underlying food anticipatory activity are still poorly understood. Here we explored the role of oxytocin (OT) and the protein c-Fos in the supraoptic nucleus (SON), medial (PVNm) and posterior (PVNp) regions of the paraventricular hypothalamic nucleus. Adult rats were assigned to one of four groups: scheduled restricted feeding (RF), ad libitum (AL), fasting after restricted feeding (RF-F), to explore the possible persistence of oscillations, or ad libitum fasted (AL-F). In the SON and in the PVNm, OT cells were c-Fos positive after food intake; in contrast, OT cells in the PVNp showed c-Fos activation in anticipation to food access, which persisted in RF-F subjects. We conclude that OT and non-OT cells of the SON and PVNm may play a role as recipients of the entraining signal provided by food intake, whereas those of the PVNp which contain motor preautonomic cells that project to peripheral organs, may be involved in the hormonal and metabolic anticipatory changes in preparation for food presentation and thus, may be part of a link between central and peripheral oscillators. In addition, due to their persistent activation they may participate in the neuronal network for the clock mechanism that leads to food entrainment.

Oxytocinergic Cells of the Posterior Hypothalamic Paraventricular Nucleus Participate in the Food Entrained Clock

The mechanisms underlying food anticipatory activity is still not well understood. Here we explored the role of oxytocin (OT) and the protein c-Fos in the supraoptic nucleus (SON) and in the medial (PVNm) and posterior (PVNp) regions of the paraventricular hypothalamic nucleus. Adult rats were assigned to one of four groups: scheduled restricted feeding (RF), Ad libitum (AL), fasting after restricted feeding (RF-F), to explore the possible persistence of oscillations, or Ad libitum fasted (AL-F). In the SON and in the PVNm, OT cells were c-Fos positive after food intake; contrasting, OT cells in the PVNp showed c-Fos activation in anticipation to food access, which persisted in RF-F subjects. We conclude that OT cells of the SON and PVNm may play a role as recipients of the entraining signal provided by food intake, whereas those of the PVNp which contain motor preautonomic cells that project to peripheral organs, may be involved in the hormonal and metabolic anticipatory changes in preparation for food presentation and thus, may be part of a link between central and peripheral oscillators. In addition, due to their persistent activation they may participate in the neuronal network for the clock mechanism that leads to food entrainment.

Temporal Memory in Foraging of the Stingless Bee Melipona subnitida (Hymenoptera: Apidae: Meliponini)

Bees feed on nectar and pollen, however these resources are often available to floral visitors during restricted temporal windows. The presence of temporal memory is an advantage, as foragers can save energy by scheduling their flight activity to coincide with peaks of nectar secretion in the flowers or at times of higher sugar concentration in the nectar. Thus, the objectives of this study were (i) to investigate whether Melipona subnitida has temporal memory, and evaluate whether it becomes more accurate over the days, and (ii) to determine whether the behavior of anticipating the offered resource presents intra-individual consistency in the behavior of foragers. The visitation of the bees was high before and during the opening interval of the food resource, but rare after the closing, suggesting that M. subnitida has the ability to memorize the time of availability of the resource, increasing the accuracy over the days, with bees anticipating their visits in relation to the time they discovered the resource, and the opening time of the resource. There was individual consistency in the behavior of food-anticipatory activity, with the presence of bees that consistently anticipated in relation to the opening time of the resource (inspectors) and bees that consistently did not anticipate (reactivated forager) . By anticipating the search for a resource, foragers allow the group to exploit it effectively, as they exploit it in the first hours of its opening, and foragers that never anticipate avoid unnecessary risks of predation and energy expenditure.

The Hepatic Monocarboxylate Transporter 1 (MCT1) Contributes to the Regulation of Food Anticipation in Mice

Daily recurring events can be predicted by animals based on their internal circadian timing system. However, independently from the suprachiasmatic nuclei (SCN), the central pacemaker of the circadian system in mammals, restriction of food access to a particular time of day elicits food anticipatory activity (FAA). This suggests an involvement of other central and/or peripheral clocks as well as metabolic signals in this behavior. One of the metabolic signals that is important for FAA under combined caloric and temporal food restriction is β-hydroxybutyrate (βOHB). Here we show that the monocarboxylate transporter 1 (Mct1), which transports ketone bodies such as βOHB across membranes of various cell types, is involved in FAA. In particular, we show that lack of the Mct1 gene in the liver, but not in neuronal or glial cells, reduces FAA in mice. This is associated with a reduction of βOHB levels in the blood. Our observations suggest an important role of ketone bodies and its transporter Mct1 in FAA under caloric and temporal food restriction.

Behavioral and stress responses to feeding time in pregnant sows under limit-fed regime

We investigated the effect of feeding time on behavior and stress responses in pregnant sows under isocaloric conditions. Twenty-four sows were balanced for parity and randomly assigned to 1 of 3 feeding times. Corn-soybean meal-based diet was fed once at: 0730 (Control, T1), 1130 (T2), and 1530 h (T3). On average, sows received 7062 kcal ME/d from 2.20 kg of diet formulated to contain SID Lys/ME of 1.71 g/Mcal. The study was conducted for 28 days (21 d acclimation to the feeding regime and 7 days data collection). Saliva samples were collected every 2 hours for 12 hr in stalls on day 52 of pregnancy. Behavior data were collected 24 hr for 7 d from day 53 of gestating by affixing a remote insights ear tag to each sow. Each sow had 120,960 data points categorized into: "Active", "Feed" or "Dormant". Due to housing constraint, all sows were housed in individual stalls in the same barn presenting a potential limitation of the study. Data were analyzed using PROC MIXED and GLIMMIX procedures of SAS 9.4 for cortisol and behavior data, respectively. Sow was the experimental unit. The area under the curve (AUC) is quantitative evaluation of response as threshold varies over all possible values. A 12-hr cortisol total area under the curve (AUC) for sows fed once daily at 1130 h was reduced relative to sow group fed at 1530 h (P = 0.046) but similar compared with the control sows (P = 0. 323). The control sows (0730 h) had reduced total (P < 0.001) and feeding (P = 0.001) activity AUCs relative to sows on 1130 but did not differ compared with sows on 1530 h feeding schedules (P > 0.100). Sows on 1130 h feeding schedule had greater feed anticipatory activity (FAA), 24-hr total activity count, total (P < 0.001) and feeding (P < 0.001) activity AUC compared with sows fed daily at 1530 h. In conclusion, feeding pregnant sows earlier in the morning (0730 h) appears to minimize sows’ behavior but similar cortisol response. Sows on 1130 h feeding schedule had greater activities but reduced cortisol concentration, suggesting that elevated sow activity might not necessarily indicate activation of hypothalamic-pituitary-adrenal axis.

Food Entrainment, Arousal, and Motivation in the Neonatal Rabbit Pup

In the newborn rabbit, the light entrainable circadian system is immature and once a day nursing provides the primary timing cue for entrainment. In advance of the mother’s arrival, pups display food anticipatory activity (FAA), and metabolic and physiological parameters are synchronized to this daily event. Central structures in the brain are also entrained as indicated by expression of Fos and Per1 proteins, GFAP, a glial marker, and cytochrome oxidase activity. Under fasting conditions, several of these rhythmic parameters persist in the periphery and brain, including rhythms in the olfactory bulb (OB). Here we provide an overview of these physiological and neurobiological changes and focus on three issues, just beginning to be examined in the rabbit. First, we review evidence supporting roles for the organum vasculosum of lamina terminalis (OVLT) and median preoptic nucleus (MnPO) in homeostasis of fluid ingestion and the neural basis of arousal, the latter which also includes the role of the orexigenic system. Second, since FAA in association with the daily visit of the mother is an example of conditioned learning, we review evidence for changes in the corticolimbic system and identified nuclei in the amygdala and extended amygdala as part of the neural substrate responsible for FAA. Third, we review recent evidence supporting the role of oxytocinergic cells of the paraventricular hypothalamic nucleus (PVN) as a link to the autonomic system that underlies physiological events, which occur in preparation for the upcoming next daily meal. We conclude that the rabbit model has contributed to an overall understanding of food entrainment.