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Maternal care is a motivated behavior and in the rabbit it is restricted to the spontaneous return of the mother to nurse her pups for just a few minutes once a day. Previously we have reported neural activation of brain areas and neuroendocrine cells after nursing. However, this daily spontaneous return suggests that the mother is in a high motivational state to nurse her pups. Here we hypothesized that during anticipation of nursing there is an activation of dopaminergic neurons of the mesolimbic system and in their target areas. Then we explored, by the expression of FOS protein, possible activation of the mesolimbic system as well as dopaminergic cells of the A10 cell group before and after nursing and in control does. Additionally, we measured FOS expression in the preoptic area and lateral septum. We found a significant increase of FOS before nursing, and a further increase after nursing, in the mesolimbic system and dopaminergic cells as well as in the preoptic area and lateral septum. Interestingly, the medial prefrontal area shows an intense activation during anticipation of nursing, which remains after nursing. We conclude that the activation of the mesolimbic system before nursing is related to the high locomotor behavior prior to the next nursing bout and support the proposal that the mother is in a high motivational state at the time of returning to the nest. The additional activation after nursing can be related to the neuroendocrine and neural consequences of the milk ejection reflex by suckling., (© 2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)

Maternal behavior in the rabbit is restricted to a brief nursing period every day. Previously, we demonstrated that this event induces daily rhythms of Period1 (PER1) protein, the product of the clock gene Per1, in oxytocinergic and dopaminergic populations in the hypothalamus of lactating rabbit does. This is significant for the periodic production and ejection of milk, but the activation of other areas of the brain has not been explored. Here, we hypothesised that daily suckling would induce a rhythm in the preoptic area, lateral septum, and bed nucleus of the stria terminalis, which are important areas for the expression of maternal behavior in mammals, including the rabbit. To this end, we analysed PER1 expression in those areas through a complete 24-h cycle at lactation day 7. Does were scheduled to nurse during either the day at 10:00 h [zeitgeber time (ZT)03] or the night at 02:00 h (ZT19). Non-pregnant, non-lactating females were used as controls. In contrast to control females, lactating does showed a clear, significant rhythm of PER1 that shifted in parallel with the timing of nursing in the preoptic area and lateral septum. We determined that the maximal expression of PER1 at 8 h after scheduled nursing decreased significantly at 24 and 48 h after the absence of suckling. This effect was more pronounced in the lateral septum than in the preoptic area. We conclude that daily suckling is a powerful stimulus inducing rhythmic activity in brain structures in the rabbit that appear to form part of a maternal entrainable circuit., (© 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)

Rabbit pups represent a natural model of food anticipatory activity (FAA). FAA is the behavioral output of a putative food entrainable oscillator (FEO). It had been suggested that the FEO is comprised of a distributed system of clocks that work in concert in response to gastrointestinal input by food. Scheduled food intake synchronizes several nuclei in the brain, and the hypothalamus has received particular attention. On the contrary, brainstem nuclei, despite being among the brain structures to first receive food cues, have been scarcely studied. Here we analysed by immunohistochemistry possible oscillation of FOS and PER1 proteins through a complete 24-h cycle in the dorsal vagal complex (DVC) and parabrachial nucleus (PBN) of 7-8-day-old rabbit pups scheduled to nurse during the night (02:00 h) or day (10:00 h), and also in fasted subjects to explore the possible persistence of oscillations. We found a clear induction of FOS that peaks 1.5 h after nursing in all nuclei studied. PER1 was only synchronized in the PBN, reaching highest values 12 h after nursing. Only PER1 oscillations persisted, with a shift, in fasted subjects. We conclude that the DVC nuclei are probably more related to the transmission of food cues to other brain regions, but that the PBN participates in the integration of information essential for FAA. Our results support previous findings suggesting that the DVC nuclei, but not PBN, are not essential for FAA. We suggest that PBN is a key component of the proposed distributed system of clocks involved in FAA., (© 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd.)

Nursing in the rabbit is under circadian control, and pups have a daily anticipatory behavioral arousal synchronized to this unique event, but it is not known which signal is the main entraining cue. In the present study, we hypothesized that food is the main entraining signal. Using mother-deprived pups, we tested the effects of artificial feeding on the synchronization of locomotor behavior, plasma glucose, corticosterone, c-Fos (FOS) and PERIOD1 (PER1) rhythms in suprachiasmatic, supraoptic, paraventricular and tuberomammillary nuclei. At postnatal day 1, an intragastric tube was placed by gastrostomy. The next day and for the rest of the experiment, pups were fed with a milk formula through the cannula at either 02:00 h or 10:00 h [feeding time = zeitgeber time (ZT)0]. At postnatal days 5-7, pups exhibited behavioral arousal, with a significant increase in locomotor behavior 60 min before feeding. Glucose levels increased after feeding, peaking at ZT4-ZT12 and then declining. Corticosterone levels were highest around the time of feeding, and then decreased to trough concentrations at ZT12-ZT16, increasing again in anticipation of the next feeding bout. In the brain, the suprachiasmatic nucleus had a rhythm of FOS and PER1 that was not significantly affected by the feeding schedule. Conversely, the supraoptic, paraventricular and tuberomammillary nuclei had rhythms of both FOS and PER1 induced by the time of scheduled feeding. We conclude that the nursing rabbit pup is a natural model of food entrainment, as food, in this case milk formula, is a strong synchronizing signal for behavioral, hormonal, metabolic and neural parameters., (© 2011 The Authors. European Journal of Neuroscience © 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd.)

Mother rabbits nurse their young once a day with circadian periodicity. Nursing bouts are brief (ca. 3 min) and occur inside the maternal burrow. Despite this limited contact mother rabbits and their pups are tuned to each other to ensure that the capacities of each party are used efficiently to ensure the weaning of a healthy litter. In this review we present behavioral, metabolic and hormonal correlates of this phenomenon in mother rabbits and their pups. Research is revealing that the circadian rhythm of locomotion shifts in parallel to the timing of nursing in both parties. In pups corticosterone has a circadian rhythm with highest levels at the time of nursing. Other metabolic and hormonal parameters follow an exogenous or endogenous rhythm which is affected by the time of nursing. In the brain, clock genes and their proteins (e.g. Per1) are differentially expressed in specific brain regions (e.g. suprachiasmatic nucleus, paraventricular nucleus) in relation to providing or ingesting milk in mothers and young, respectively. These findings suggest that circadian activities are modulated, in the mothers, by suckling stimulation and, in the young, by the ingestion of milk and/or the perception of the mammary pheromone. In conclusion, the rabbit pup is an extraordinary model for studying the entraining by a single daily food pulse with minimal manipulations. The mother offers the possibility of studying nursing as a non-photic synchronizer, also with minimal manipulation, as suckling stimulation from the litter occurs only once daily.

Nursing in the rabbit is a circadian event during which mother and pups interact for a period of < 5 min every day. Here we explored behavioral and neuronal changes in the mother by analyzing the suprachiasmatic nucleus (SCN), and oxytocinergic (OT) neurons in the paraventricular nucleus (PVN) and the supraoptic nucleus (SON). We maintained lactating does in a light-dark cycle (lights on at 07 : 00 hours; ZT0); they were scheduled to nurse during either the day (ZT03) or the night (ZT19). Groups of intact and nursing females was perfused, one at each 4-h point through a 24-h cycle. We explored, by immunohistochemistry, the PER1 expression and double-labeling, with OT antibody, of neurons in the PVN and SON at lactation on day 7. In the SCN, intact and lactating groups had peak PER1 expression at ZT11; however, there was a reduction in PER1 at peak time in the nursing groups. There was a locomotor activity rhythm with increased activity around the time of lights-on in intact subjects and around the time of suckling in lactating does. There was an induction of PER1 in OT cells in the PVN and SON that shifted in phase with timing of nursing. We further explored the maintenance of the PER1 expression in OT cells in nursing-deprived does and found a significant decrease at 24 and 48 h after the last nursing. We conclude that suckling induced PER1 in the PVN and SON, but not in the SCN, in nursing does, and also shifted their locomotor behavior.

In nature and under laboratory conditions, dams nurse rabbit pups once daily for a duration of fewer than 5 min. The present study explored neural mechanisms mediating the timing of nursing in this natural model of food anticipatory activity, focussing on the suprachiasmatic nucleus (SCN), the locus of the master circadian clock and on the dorsomedial hypothalamic nucleus (DMH), a region implicated in timing of food-entrained behavior. Rabbit pups are born in the dark, with eyelids closed. Nursing visits to the litters also occurs during the dark phase. To explore the effect of the timing of feeding, pups were maintained in constant darkness, while females housed in a light-dark cycle were permitted to nurse their pups either during the night (night-fed group) or day (day-fed group). All pups exhibited anticipatory locomotor activity before daily nursing. In the SCN, PER1 and FOS peaked during the night in both groups, with a longer duration of elevated protein expression in the night-fed group. In contrast, DMH peak PER1 expression occurred 8 h after pups were fed, corresponding to the shift in timing of nursing. Comparison of nursed and 48 h fasted pups indicates that the timing of PER1 expression was similar in the SCN and DMH, with fewer PER1-positive cells in the latter group. The results indicate that rabbit pups show food anticipatory activity, and that timing of nursing differentially affects PER1 expression in the SCN and DMH.