Invited Symposium: Maternal Behaviour



Materials & Methods


Discussion & Conclusion



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Activation Of Fos-Like Immunoreactivity In The Accesory Olfactory Bulbs Folowing Induction Of Maternal Behavior In Prenatally Stressed Rats.

Contact Person: M.C.R. Del Cerro (delcerro@cu.uned.es)


Maternal behavior (MB) ensures that immature individuals will survive to adulthood. Mother rats provide their pups with heat, food and cares specifically aimed to their survival immediately after parturition. MB includes pronurturant activities, such as nest building, retrieval and licking, which precede prolonged periods of quiescent nursing. In the rat, maternal care is under hormonal control (see Numan, 1994. for Review). However, continuous exposure to pups can elicit this behavior after several days in virgin females and naive male rats (Rosenblatt, 1967).

The sexually dimporhic Vomeronasal System (VNS) (Segovia and Guillamón, 1993; 1996) is implicated in the control of MB (Fleming et al., 1979). Electrolytical lesions of structures of the VNS, have been proved to alter MB (Del Cerro et al., 1991; Izquierdo et al., 1992). Administration of Picrotoxine (a GABAa antagonist) during early postnatal periods has resulted in morphological alterations of the Accessory Olfactory Bulb (AOB), a structure belonging to the VNS, as well as in the induction of MB (Segovia et al., 1996). Olfactory imput from the AOB reaches the Ventral Bed Nucleus of the Stria Terminalis (BNST) (Winans and Scalia, 1975; Davis et al., 1978) and from this nucleus direct projections to the Medial Preoptic Area (MPA) are sent (De Olmos and Ingram, 1972). Neurons of the MPA and the BNST express c-fos immunoreactivity in maternally behaving virgin and postpartum (Numan and Numan, 1994).

On the other hand, environmental prenatal stress (EPS) is considered a teratogenic agent, that induces hormonal changes in the pregnant mother and her pups (Ward, 1980), as well as deficiencies in the performance of induced MB in prenatally stressed female rats (Pérez-Laso et al., 1997). So, EPS increases stress-induced corticosterone secretion peak in preweaning rats (Peters, 1982; Takahashi et al., 1988) and attenuates habituation over repeated exposure to stress in the adult (Fride et al., 1986).

Since EPS may cause changes in hormonal plasmic levels, as well as alterations in maternal behavior, in this work we study wheter EPS treatment may cause changes in progesterone, corticosterone and estradiol plasmic levels and a long-lasting effect on the induction of MB, and wheter these changes are realted with c-fos-like immunoreactivity of the AOB mitral cells, in virgin female rats when adult.

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Materials and Methods

Two groups of Wistar female rats (Iffacredo, Barcelona-Spain) were formed. Control females (CF, N=16) and Prenatally stressed females (PS3-F, N=15).

The mothers of the PS3-F group were kept three times daily during 45 minutes (at 9 a.m., 13 and 17 p.m.) in a restrainer stressor device, using the Ward paradigm (Ward, 1972): restrain, light (2,500 luxes) and heat (31±1ºC), from day 14 to 20 of pregnancy. The mothers of the CF group were left undisturbed in their cages throughout gestation.

At the age of 90 days animals were tested for MB induction during 12 consecutive days. Session lenght was 10 minutes, using MBR software (Claro et al., 1994) to register the different maternal behavior patterns (Del Cerro et al., 1991).

In the CF group, animals (N=6) that reached sensitization criterion (two consecutive days performing retrieval of the whole litter), were sacrificed and their AOB removed and processed for c-fos expression. At the end of the MB test period (day 12th.), five CF rats thah did not performed MB and other five PS3-F subjects, randomly selected, were sacrificed and their AOB processed for c-fos expression. AOB mitral cells expressing c-fos were counted (x10), using and optical microscope (Diaplan Leitz).

Blood samples were collected from every group of rats and plasmic hormonal levels were determined, using a commercially available radioimmunoassay kits (Sorin Biomedical Diagnostic, Vercelli-Italy).

For statistical analysis of data, non-parametric Kruskal-Wallis test were used and post-hoc Mann-Whitney-U test was applied, for all measures, since no homogeneity of variance was found.

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- A significant increase in plasmic corticosterone and progesterone levels has been detected in PS3-F in comparison with CF (P<.000 in both cases), as well as a decrement in Estradiol (p<.000). (See Table).

BEHAVIOR. - The percentage of PS3-F rats that became maternal was significantly lower than that of CF group (p<.0000). (Fig. 1).

- The PS3-F obtained too lower nest building scores than CF group (p<.0000). (


-The number of mitral cells of the AOB expressing c-fos immunoreactivity was higher in those CF rats that became maternal, than in non-maternal CF or PS3-F subjects (p<.017 and p<.05, respectively)(See Table).

However, no significant differences were found between non-maternal CF and PS3-F female rats.

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Discussion and Conclusion

Our results clearly demonstrate that environmental prenatal stress has induced elevated plasmic corticosterone levels in the PS3-F group. These results are in agreement with the findings of Makino et al. (1994), who demonstrated that stress during pregnancy increases corticosterone levels in the pregnant mother and her fetuses, mainly in female pups.

The fact that progesterone and corticosterone levels resulted increased after PS3 treatment, but estradiol level did not, might suggest that PS3 primed the metabolic reduction pathway in decrement of the aromatization pathway.

Th poor nest building scores obtained by the PS3-F group and the absence of animals becoming maternal, in this group too, correlates with their increase of corticosterone and their decrease of estradiol levels.

Moreover, the fact that there was a correlation between c-fos expression and the display of maternal behavior indicates tha c-fos expression is dependent of the maternal behavior performance, rather than of the stress and/or the hormonal level changes.

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1. Claro, F.; Izquierdo, M.A.P.; Del Abril, A.; Segovia, S.; Guiillamón, A. and Del Cerro, M.C.R. The MBR: A computer program to record and analyze parental behavior in rodents. Physiol. Behav. 56, 5:1069-1073. 1994.

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5. Fleming, A.; Vaccarino, F.; Tambosso, L. and Cheese, P. Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203:372-374. 1979.

6. Fride, E.D.; Dan, Y.; Feldon, J.; Halevy, G.; Weinstock, M. Effects of prenatal stress in vulnerability to stress on prepuberal and adult rats. Physiol. Behav. 37:681-687. 1986.

7. Izquierdo, M.A.P.; Collado, P.; Segovia, S.; Guillamon, A. Del Cerro, M.C.R. Maternal behavior induced in male rats by bilateral lesions of the bed nucleus of the accessory olfactory tract. Physaiol. Behav. 52:707-712. 1992.

8. Makino, S.; Goild, P.W. Schulkin, J. Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amigdala and the parvocellular region of the paraventicular nucleus of the hypothalamus. Brain Res. 640:105-112. 1994.

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10. Newman, M. and Newman, M. Expression of fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav. Neurosci. 108:379-394. 1994.

11. Pérez-Laso, C.; Barona, M.L.; Haba, C.; Guillamón, A:; Segovia, S. and el Cerro, M.C.R. Environmental prenatal stress alters sex differences in parental behavior. Sixth Annual Meeting of the IBSN. San Diego (CA), April, 1997.

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14. Segovia, S.; Del Cerro, M.C.R.; Ortega, E.; Pérez-Laso, C.; Rodriguez-Záfra, M.; Izquierdo, M.A.; Guillamón, A. Role of GABAa receptorsa in the organization of brain and behavioral sex differences. NeuroReport 7:2553-2557. 1996.

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17. Takahashi, L.K.; Kalin, N.H.; Barksdale, C.M.; Van den Burght, J.A. Stressor controllability during pregnancy influences pituitary adrenal hormones concentrations and analgesic responsiveness in offspring. Physiol. Behav. 42:323-329. 1988.

18. Ward, I.L. Prenatal stress feminizes and desmasculinizes the behavior of male. Science. 175:82-84. 1972.

19. Ward, I.L. and Weisz, J. Maternal stress alters plasma testosterone in fetal males. Science. 207:328-329. 1980.

20. Weisz, J.; Brown, B.L.; Ward, I.L. Maternal stress decreases steroids aromatase activity in brain of male and female rat fetuses. Neuroendocrinology. 35:374-379. 1982.

*This study has been supported by DGYCIT PB96.0107-C03-02.

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Rodríguez-Martín, J.L.; Pérez-Laso, C.; Barona, M.L.; Ortega, E.; Guillamón, A.; Segovia, S.; Del Cerro, M.C.R.; (1998). Activation Of Fos-Like Immunoreactivity In The Accesory Olfactory Bulbs Folowing Induction Of Maternal Behavior In Prenatally Stressed Rats.. Presented at INABIS '98 - 5th Internet World Congress on Biomedical Sciences at McMaster University, Canada, Dec 7-16th. Invited Symposium. Available at URL http://www.mcmaster.ca/inabis98/cruzrdelcerro/rodriguez-martin0816/index.html
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