Abstract:We review existing knowledge of the neural, hormonal, and sensory basis of maternal aggression in the female rat. Although females may express different kinds of aggression, such as defense or dominance, the most frequent and conspicuous form of aggressive behavior among females is the one associated with motherhood. Maternal aggression occurs in various vertebrate and invertebrate species; however, our emphasis will be on maternal aggression in rats because most of the physiological investigations have been p… Show more
“…Conversely, PP19-21 dams, when tested with younger pups, changed their behavior such that they now targeted their response more towards the threat, decreasing the time spent with the pups (comparison of behavior during the matched age test with mismatched age test; behaviors towards threat: n=12, Z= −2.845, p=0.004, behaviors towards pups: Z= −2.824, p=0.005; Figure 2C), suggesting that in this case, the behavior of the dams was mostly determined by the behavior of the pups. This is in accordance with previous findings showing that maternal aggression is initially determined by the internal state of the mother but progressively becomes more dependent on the presence of the pups (Caughey et al, 2011; de Almeida et al, 2014). 10.7554/eLife.24080.005Figure 2.Maternal response is dependent on stage.( A ) Schematic of experimental design.…”
Section: Resultssupporting
confidence: 93%
“…Indeed, testing mothers at a stage mismatched with that of the pups age (PP4-6 dams with PN19-21 pups and vice versa) revealed that both the age of the pups, possibly through differences in the pups behavior (Fleming et al, 1999), and maternal PP stage, which could be caused by differences in hormonal state and/or maternal experience (Bosch and Neumann, 2008; Rosenblatt, 1967), determine maternal defensive behavior. Furthermore, we found that maternal defense is initially determined by maternal stage progressively becoming more dependent on the pups, a similar pattern to that observed for maternal aggression (Caughey et al, 2011; de Almeida et al, 2014). Further experiments are required to parse out the mediating factors of pup age on maternal defense behaviors.…”
Section: Discussionsupporting
confidence: 82%
“…From birth until weaning, many changes take place in mothers and pups. These include decreases in nursing and maternal aggression, as well as increases in the mobility of the pups (pups initially do not leave the nest and closer to weaning leave the nest frequently), and feeding behavior (pups initially are fully dependent on the mother’s milk and close to weaning eat regular food chow while still nursing) (Bolles and Woods, 1964; Caughey et al, 2011; Lonstein and Gammie, 2002; de Almeida et al, 2014). We therefore tested mothers at two postpartum (PP) stages (early, PP4-6 vs. late, PP19-21).10.7554/eLife.24080.003Figure 1.Rat dams suppress freezing when in the presence of their pups.( A ) Schematic of the experimental design.…”
Section: Resultsmentioning
confidence: 99%
“…Oxytocin (OT), a highly conserved neuropeptide, has been implicated in a number of maternal behaviors including nursing, pup retrieval and maternal aggression (Carter, 2014; Insel et al, 1998; Pedersen et al, 1992) involving brain regions such as the medial preoptic area, anteroventral periventricular nucleus of the hypothalamus, auditory cortex and lateral septum among others (Bosch et al, 2004; Leng et al, 2008; Marlin et al, 2015; de Almeida et al, 2014; Scott et al, 2015). In addition, oxytocin suppresses freezing, a conserved defense response to inescapable threats (Bale et al, 2001; Huber et al, 2005; Knobloch et al, 2012; Veenema and Neumann, 2008; Viviani et al, 2011; Windle et al, 1997; Zoicas et al, 2014).…”
When animals and their offspring are threatened, parents switch from self-defense to offspring protection. How self-defense is suppressed remains elusive. We postulated that suppression of the self-defense response, freezing, is gated via oxytocin acting in the centro-lateral amygdala (CeL). We found that rat dams conditioned to fear an odor, froze when tested alone, whereas if pups were present, they remained in close contact with them or targeted the threat. Furthermore, blocking oxytocin signaling in the CeL prevented the suppression of maternal freezing. Finally, pups exposed to the odor in the presence of the conditioned dam later froze when re-exposed alone. However, if oxytocin signaling in the dam had been blocked, pups failed to learn. This study provides a functional role for the well-described action of oxytocin in the central amygdala, and demonstrates that self-defense suppression allows for active pup protection and mother-pup interactions crucial for pup threat learning.DOI:
http://dx.doi.org/10.7554/eLife.24080.001
“…Conversely, PP19-21 dams, when tested with younger pups, changed their behavior such that they now targeted their response more towards the threat, decreasing the time spent with the pups (comparison of behavior during the matched age test with mismatched age test; behaviors towards threat: n=12, Z= −2.845, p=0.004, behaviors towards pups: Z= −2.824, p=0.005; Figure 2C), suggesting that in this case, the behavior of the dams was mostly determined by the behavior of the pups. This is in accordance with previous findings showing that maternal aggression is initially determined by the internal state of the mother but progressively becomes more dependent on the presence of the pups (Caughey et al, 2011; de Almeida et al, 2014). 10.7554/eLife.24080.005Figure 2.Maternal response is dependent on stage.( A ) Schematic of experimental design.…”
Section: Resultssupporting
confidence: 93%
“…Indeed, testing mothers at a stage mismatched with that of the pups age (PP4-6 dams with PN19-21 pups and vice versa) revealed that both the age of the pups, possibly through differences in the pups behavior (Fleming et al, 1999), and maternal PP stage, which could be caused by differences in hormonal state and/or maternal experience (Bosch and Neumann, 2008; Rosenblatt, 1967), determine maternal defensive behavior. Furthermore, we found that maternal defense is initially determined by maternal stage progressively becoming more dependent on the pups, a similar pattern to that observed for maternal aggression (Caughey et al, 2011; de Almeida et al, 2014). Further experiments are required to parse out the mediating factors of pup age on maternal defense behaviors.…”
Section: Discussionsupporting
confidence: 82%
“…From birth until weaning, many changes take place in mothers and pups. These include decreases in nursing and maternal aggression, as well as increases in the mobility of the pups (pups initially do not leave the nest and closer to weaning leave the nest frequently), and feeding behavior (pups initially are fully dependent on the mother’s milk and close to weaning eat regular food chow while still nursing) (Bolles and Woods, 1964; Caughey et al, 2011; Lonstein and Gammie, 2002; de Almeida et al, 2014). We therefore tested mothers at two postpartum (PP) stages (early, PP4-6 vs. late, PP19-21).10.7554/eLife.24080.003Figure 1.Rat dams suppress freezing when in the presence of their pups.( A ) Schematic of the experimental design.…”
Section: Resultsmentioning
confidence: 99%
“…Oxytocin (OT), a highly conserved neuropeptide, has been implicated in a number of maternal behaviors including nursing, pup retrieval and maternal aggression (Carter, 2014; Insel et al, 1998; Pedersen et al, 1992) involving brain regions such as the medial preoptic area, anteroventral periventricular nucleus of the hypothalamus, auditory cortex and lateral septum among others (Bosch et al, 2004; Leng et al, 2008; Marlin et al, 2015; de Almeida et al, 2014; Scott et al, 2015). In addition, oxytocin suppresses freezing, a conserved defense response to inescapable threats (Bale et al, 2001; Huber et al, 2005; Knobloch et al, 2012; Veenema and Neumann, 2008; Viviani et al, 2011; Windle et al, 1997; Zoicas et al, 2014).…”
When animals and their offspring are threatened, parents switch from self-defense to offspring protection. How self-defense is suppressed remains elusive. We postulated that suppression of the self-defense response, freezing, is gated via oxytocin acting in the centro-lateral amygdala (CeL). We found that rat dams conditioned to fear an odor, froze when tested alone, whereas if pups were present, they remained in close contact with them or targeted the threat. Furthermore, blocking oxytocin signaling in the CeL prevented the suppression of maternal freezing. Finally, pups exposed to the odor in the presence of the conditioned dam later froze when re-exposed alone. However, if oxytocin signaling in the dam had been blocked, pups failed to learn. This study provides a functional role for the well-described action of oxytocin in the central amygdala, and demonstrates that self-defense suppression allows for active pup protection and mother-pup interactions crucial for pup threat learning.DOI:
http://dx.doi.org/10.7554/eLife.24080.001
“…By contrast, few studies have developed a female model of depression (Chaouloff, 2013; Hammels et al, 2015). Previously, we have shown that female social defeat stress by use of maternal aggression, in which a lactating dam shows defensive aggression toward unfamiliar intruders (de Almeida et al, 2014), induces anhedonia-like responses, disrupts estrous cycle, and alters dopaminergic and behavioral responses to psychostimulants, including cocaine (Miczek et al, 2011a; Shimamoto et al, 2011, 2014). …”
Background: Women are twice as likely as men to develop major depression. The brain mechanisms underlying this sex disparity are not clear. Disruption of the glutamate–glutamine cycle has been implicated in psychiatric disturbances. This study identifies sex-based impairments in the glutamate–glutamine cycle involving astrocytes using an animal model of depression.Methods: Male and female adult Long-Evans rats were exposed to chronic social defeat stress (CSDS) for 21 days, using a modified resident-intruder paradigm. Territorial aggression was used for males and maternal aggression was used for females to induce depressive-like deficits for intruders. The depressive-like phenotype was assessed with intake for saccharin solution, weight gain, estrous cycle, and corticosterone (CORT). Behaviors displayed by the intruders during daily encounters with residents were characterized. Rats with daily handling were used as controls for each sex. Ten days after the last encounter, both the intruders and controls were subjected to a no-net-flux in vivo microdialysis to assess glutamate accumulation and extracellular glutamine in the nucleus accumbens (NAc). The contralateral hemispheres were used for determining changes in astrocytic markers, including glial fibrillary acidic protein (GFAP) and glutamate transporter-1 (GLT-1).Results: Both male and female intruders reduced saccharin intake over the course of CSDS, compared to their pre-stress period and to their respective controls. Male intruders exhibited submissive/defensive behaviors to territorial aggression by receiving sideways threats and bites. These males showed reductions in striatal GLT-1 and spontaneous glutamine in the NAc, compared to controls. Female intruders exhibited isolated behaviors to maternal aggression, including immobility, rearing, and selfgrooming. Their non-reproductive days were extended. Also, they showed reductions in prefrontal and accumbal GFAP+ cells and prefrontal GLT-1, compared to controls. When 10 μM of glutamate was infused, these females showed a significant accumulation of glutamate compared to controls. Infusions of glutamate reduced extracellular glutamine for both male and female intruders compared to their respective controls.Conclusion: Twenty-one days of territorial or maternal aggression produced a depressive-like phenotype and impaired astrocytes in both male and female intruders. Disruption of the glutamate–glutamine cycle in the PFC-striatal network may be linked to depressive-like deficits more in females than in males.
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