Elsevier

Neuroscience

Volume 133, Issue 2, 2005, Pages 359-369
Neuroscience

Behavioural neuroscience
Mapping of brain networks involved in consolidation of lamb recognition memory

https://doi.org/10.1016/j.neuroscience.2005.02.027Get rights and content

Abstract

In sheep, ewes at parturition are responsive to any newborn lamb, but within less than 1 h, mothers learn to recognize the odor of their lamb and restrict maternal care to their own offspring (maternal selectivity). In a first experiment, we investigated the long-term retention of maternal selectivity after various mother-young contact and separation durations. After 4 h of contact, 36 h of separation leads to a total loss of selectivity. Increasing contact duration to 7 days prior to this separation maintains selectivity. These data suggest that lamb memory after going through an initial labile state after parturition, is consolidated over time into a more stable long-term memory. Fos immunohistochemistry reveals that reintroduction of the lamb after 4 h of mother-young contact and 3 h of separation activates different maternal brain regions than reintroduction of the lamb after 7 days of mother-young contact and 3 h of separation. While the piriform cortex shows an enhanced activation at both times, a selective enhancement of activation is observed in the frontal medial and orbitofrontal cortices only after 7 days of mother-young contact. These data suggest that as consolidation occurs, the neurobiological networks sustaining lamb memory involve different structures.

Section snippets

Experiment 1: maintenance of lamb recognition after various mother-young contact and separation durations

In this first experiment, we studied the effects of various durations of mother-young separations (from 3 h to 72 h) following different periods of postpartum contact (from 4 h to 7 days) on olfactory recognition of the familiar lamb. We also looked at maternal responsiveness since we had previously observed that ewes separated from their lambs also show a loss of maternal care toward their own young (Lévy et al., 1991). We hypothesized that both maternal responsiveness and recognition of the

Maternal responsiveness

Some ewes were not maternal at the end of the separation and rejected both familiar and unfamiliar lambs. Retention performances of maternal responsiveness appeared to be mainly dependent on the separation duration, whereas time of contact prior to separation had no effect. After 4 h of mother-young contact, the proportion of maternal ewes did not differ significantly between 3 h and 6 h of mother-young separation (Fig. 1A). This proportion was significantly lower when the duration of the

Discussion

Data from this experiment show that maintenance of maternal responsiveness and selectivity are differently affected by the duration of mother-young contact and separation.

A rapid fading of maternal responsiveness with increasing separation length was observed. An increase of mother-young contact cannot compensate for this decline. This fall of maternal responsiveness in ewes separated from their lambs for 36 or 72 h might be related to the fact that experimenters held ewes while alien lambs

Experimental procedures

Eighteen multiparous Ile-de-France ewes were housed individually (2× 1 m) 1 week before parturition. Parturition was synchronized as described in the first experiment. At lambing, only one lamb was left with its mother to standardize litter size. Four groups of ewes were studied. In two experimental groups, mothers were separated from their lamb for 3 h, after either 4 h of contact (n=5) or 7 days of contact (n=6). The lambs were reunited with their mother for 2 h, this period allowing maximal

Results

For all the structures, no difference between both control groups was observed (4 h or 7 days of contact followed by 5 h of separation). Consequently, these groups were pooled in a single control group (n=7).

Discussion

Our experiment explored brain networks activated during retrieval of lamb olfactory memory performed under a labile or a consolidated memory state. While previous studies have shown that during memory formation, extensive activation is found throughout the olfactory processing network (Da Costa et al 1997, Keller et al 2004a), our results suggest that there are only a few brain structures engaged in retrieval of lamb recognition memory.

Acknowledgments

We thank Francis Dupont and the shepherds for the care they provided to the animals. We are also grateful to Francis Paulmier and the whole staff of the hospital for experimental facilities, and especially to Christian Moussu and Jean-Philippe Dubois for their nocturnal assistance. The help of Nicole Jouaneau, Gérard Vénier and Eric Archer was greatly appreciated during the experiments. We thank Guillaume Ferreira and Anne-Marie Mouly for critical reading as well as Raymond Nowak and Sue Edrich

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