Maternal behavior of the mouse dam toward pups: implications for maternal separation model of early life stress

Abstract

Maternal care is essential for an adequate pup development, as well as for the health of the dam. Exposure to stress in early stages of life can disrupt this dam-pup relationship promoting altered neurobiological and behavioral phenotypes. However, there is a lack of consensus regarding the effects of daily maternal separation (MS) on the pattern of maternal behavior. The aim of this study is to compare the patterns of maternal behavior between mice exposed to MS and controls. BALB/c mice were subjected to MS for a period of 180 min/day from postnatal day 2-7 (n = 17) or designated to be standard animal facility reared (AFR) controls (n = 19). Maternal behaviors were computed as frequency of nursing, licking pups and contact with pups, and nonmaternal behaviors were computed as frequency of actions without interaction with pups and eating/drinking. A total of 18 daily observations of maternal behavior were conducted during these six days, and considering the proportion of maternal and nonmaternal behaviors, an index was calculated. There was no difference when comparing the global index of maternal behavior between the AFR and MS animals by the end of the observed period. However, the pattern of maternal behavior between groups was significantly different. While MS dams presented low frequency of maternal behavior within the first couple days of the stress protocol, but increasing over time, AFR dams showed higher maternal behavior at the beginning, reducing over time. Together, our results indicate that MS alters the maternal behavior of the dams toward pups throughout the first week of the stress protocol and provoked some anxiety-related traits in the dams. The inversion of maternal behavior pattern could possibly be an attempt to compensate the low levels of maternal care observed in the first days of MS.

Chronic psychosocial stress during pregnancy affects maternal behavior and neuroendocrine function and modulates hypothalamic CRH and nuclear steroid receptor expression

“…Importantly, we hypothesize brief periods of pup separation during neuroendocrine and behavioral assays in our study did not significantly contribute to our stress paradigm. Previous studies have shown brief pup separation is not a sufficient stressor to increase maternal HPA axis activity or result in depressive-like behaviors during midto-late lactation 27,[70][71][72][73] . Nevertheless, future studies are needed to determine the precise effect of pup removal on early postpartum neuroendocrine activity and behavior.…”

Targeting the Stress System During Gestation: Is Early Handling a Protective Strategy for the Offspring?

“…For instance, poor parental ties are usually associated with increased risk for several psychological vulnerabilities, whereas an increase in parental care improved behavioral outcomes, cognitive performance and also boost resiliency to stress (Canetti et al, 1997;Meaney, 2001;Kaffman and Meaney, 2007). Accordingly, early handling procedure, consisting in a short maternal separation of the mother from the pups, represents a particular event for the dam that is able to produce higher level of interest by the mother in the offspring and, in turn, elicits more maternal care upon reunion (Rees and Fleming, 2001;Kosten and Kehoe, 2010;Zimmerberg and Sageser, 2011;Own and Patel, 2013;Orso et al, 2018). These observations are consistent with those obtained in the present research where the effects on the maternal-infant dyad were investigated.…”

Influencia del estrés en la conducta maternal en hembras de ratón

“…Las madres no separadas en los primeros días mostraban un comportamiento maternal alto, pero este iba disminuyendo; en cambio, las madres separadas primero mostraban un comportamiento maternal bajo que aumentaba con el paso de los días. Esta evaluación del comportamiento maternal se llevó a cabo durante 6 días con un total de 18 observaciones (Orso et al 2018). Discusión La influencia del estrés en la conducta maternal es un campo que precisa mayor investigación, pues mucho es sabido sobre el efecto que provoca el estrés en las primeras etapas de la vida de las crías y en su posterior desarrollo adulto, pero mucha menos investigación existe hasta la fecha sobre el efecto que el estrés produce en el circuito neural que induce la conducta maternal.…”

“…Por último, y siendo el dato más novedoso y relevante para nuestro estudio, se ha observado que la separación materno-filial provoca cambios en el patrón comportamental de las madres, ya que las madres que han sido separadas de sus crías muestran un patrón de cuidado mucho más ansioso, siendo sobreprotectoras a lo largo del tiempo, algo que no se observa en madres no separadas (Orso et al 2018). En ratas, se ha demostrado que la maternidad provoca cambios en la expresión de CRF cerebral provocando que las madres presenten una mejor respuesta al estrés, bajada de ansiedad y control del miedo (Stern, Goldman y Levine 1973; Bitran, Hilvers y Kellogg 1991), tratándose de una respuesta totalmente adaptativa para llevar a cabo la crianza.…”

“…En ratas, se ha demostrado que la maternidad provoca cambios en la expresión de CRF cerebral provocando que las madres presenten una mejor respuesta al estrés, bajada de ansiedad y control del miedo (Stern, Goldman y Levine 1973; Bitran, Hilvers y Kellogg 1991), tratándose de una respuesta totalmente adaptativa para llevar a cabo la crianza. En ratones, sin embargo, es posible que, al inducir una separación materno-filial de 3 horas, la expresión de CRF se vea modifica y esto provoque un cambio en la respuesta a estímulos estresantes y, en consecuencia, cambios en el estilo maternal, volviéndose este mucho más sobreprotector a lo largo del tiempo, que es precisamente lo que observamos en este estudio (Orso et al 2018).…”