Effects of electrical lesions of the medial preoptic area and the ventral pallidum on mate-dependent paternal behavior in mice
Introduction
Most of our knowledge of mammalian parental behavior is based on studies of mother–infant interactions. There is evidence supporting the hypothesis that the mammalian father is an important participant and contributor to the care and development of offspring [1], [2], [3], [4]. However, this behavior is dependent on the species, as most mammalian fathers exhibit notably little paternal care, and only a small portion exhibit full/obligatory paternal care [3], [5], [6], [7], [8], [9], [10]. Parental behavior of rodents is defined as behavior directed toward offspring that increases their survival (e.g., nurturing, nesting, and retrieving) [5], [6]. The significance of such paternal care, particularly because not all species exhibit paternal care, has been an area of debate. This uncertainty could be partially resolved by examining the neuroanatomical and molecular substrates and neurocircuitry associated with such paternal behavior. Such studies could provide some significant findings to understand human male parental behavior and social interaction, which contribute to developmental psychiatric diseases, including autism and schizophrenia [9], [11], [12], although there is a wide gap between animal models and humans.
There are several (widely used) laboratory mouse strains that exhibit varying levels of spontaneous paternal care – some are in fact quite paternal [2], [3], [6], [8], [13]. However, uniparental male mice that are forced to live together exhibit maternal-like behavior, including providing protection and warmth to offspring [13]. We recently developed a co-housing paradigm to study paternal behavior of the mouse ICR strain [14], [15], [16]. When mouse sires are continuously housed in the maternal cage with their mates and pups for three to five days prior to and after parturition, they exhibit signs of maternal-like parental care. Furthermore, when separated from their pups for 10 min and co-housed with the dam in a new cage, sires exhibited retrieval behavior when reunited with their pups [14]. We also found that expression of male parental behavior is triggered by olfactory and unique 38-kHz ultrasonic auditory signals to the sire from the mate dam. Thus, we defined this behavior displayed in the ICR male mice as mate-dependent paternal behavior induced by the interactive communication from the dam to the sire.
Although we have identified several conditions that elicit mate-dependent paternal behavior, little is known about the neurocircuitry responsible for this behavior. We recently reported that central cholinergic cellular signaling [15] and CD38 and oxytocin signaling in the nucleus accumbens (NAcc) [16] are critical for the expression of paternal care. However, it is not yet known if the brain regions responsible for maternal behavior, the medial preoptic area (mPOA), the ventral tegmental area (VTA), the NAcc and the ventral pallidum (VP), also regulate paternal behavior [5], [6], [17], [18]. To address this issue, we use a classical deletion method, the electrolytic brain lesion (EBL) technique, according to the details described by Lee and Brown [26], to determine the extent to which the mPOA and VP regions regulate paternal care in mice of the ICR strain [19], since we hypothesize that the brain lesions may affect paternity. We first focus on paternal behavior by lesioned sires mated with intact dams, because sires isolated alone do not display paternal behavior, dams inevitably care pups, and dams are needed for sires to induce paternal care [14]. Next, we test pup care behavior and pup survival in the sire plus dam lesion groups to confirm if they are behaviorally different from the sire-only-lesion groups. Finally, we use sires of non-treated or sham-operated sires as a control experiment.
Section snippets
Animals
Males and females of the Slc:ICR line were obtained from Japan SLC Inc. (Hamamatsu, Japan) and kept in our laboratory, as described previously [14], [19]. Virgin males and females were paired on postnatal days 45–55. All experiments were approved by the Committee on Animal Experimentation of Kanazawa University.
Electrical brain lesion procedure
After seven days of mating, both mice of a given mating pair or only the male counterpart underwent bilateral EBL or sham lesions to the mPOA or VP regions. Mice were anesthetized with
Results
Fig. 1 depicts representative tissue damage with acceptable bilateral EBLs of the mPOA (Fig. 1A) or VP (Fig. 1B) regions. Bilateral mPOA lesions were mostly located in the anterior, lateral and medial parts of the mPOA. Bilateral VP lesions were located in the anterior, medial and posterior parts of the VP.
The sires with the bilateral EBL of the mPOA (n = 10) or VP (n = 5) did not display the mate-dependent retrieval behavior upon reunion with pups after separation (Table 1, the second and fifth
Discussion
The present results indicate that the mPOA and VP regions are important for paternal retrieval behavior in mouse strains that exhibit mate-dependent paternal behavior [14]. In this study, we also demonstrated that the sires subjected to EBL of the mPOA or the VP exhibit severe deficits in other components of parental behavior, including grooming and crouching. We also found that dams subjected to EBL of the mPOA or the VP also exhibit deficits in nurturing behavior. The lesioned sires were
Acknowledgment
This work was supported in part by the Strategic Research Program for Brain Sciences from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.
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2021, Encyclopedia of Behavioral Neuroscience: Second EditionOxytocin and CD38 in the paraventricular nucleus play a critical role in paternal aggression in mice
2020, Hormones and BehaviorCitation Excerpt :However, we have previously shown that the ICR male mouse displays intensive parental behavior, even though it is not monogamous (Jin et al., 2007; Liu et al., 2013). Our previous results showed that the neural circuitry mediating this type of paternal nurturing behavior includes the medial preoptic area (mPOA), the nucleus accumbens (NAcc), and the ventral pallidum (VP; Akther et al., 2014), suggesting that paternal nurturing behavior is mediated by the same brain regions that mediate maternal nurturing behavior, as proposed by Numan and his colleagues (Numan, 2015; Numan and Stolzenberg, 2009; Numan and Young, 2016). Therefore, the principal aim of this study was to determine whether the mechanism or the neurocircuits for paternal aggression are similar to those for maternal aggression.
Experience-dependent mechanisms in the regulation of parental care
2019, Frontiers in NeuroendocrinologyMore than just mothers: The neurobiological and neuroendocrine underpinnings of allomaternal caregiving
2019, Frontiers in NeuroendocrinologyCitation Excerpt :Lesions to the MPOA and NAcc, and to a lesser extent the basolateral amygdala (BLA), of the biparental California mouse reduced parental behaviors in males (Lee and Brown, 2007). Bilateral cMPOA and/or VP lesions abolish allomaternal behavior (Akther et al., 2014; Tsuneoka et al., 2015) – an effect that also promotes infanticidal behavior in male C57BL/6J mouse fathers (Tsuneoka et al., 2015). Collectively, these studies suggest that the MPOA-VTA-NAcc-VP neural circuit may be involved in paternal behavior.