Biology subjects

Marler, C. A.

Publications and source records attributed to Marler, C. A..

6 recordsLinked to original sources

bioRxiv2025

Sex Differences in Structural and Receptor mRNA Expression in the Ventral Anterior Cingulate Cortex and a Potential Role of Perineuronal Nets in Monogamous Pair Bond Establishment (Peromyscus californicus)

The monogamous California mouse (Peromyscus californicus) exhibits distinct behavioral changes during pair bond formation. Using a detailed temporal behavioral analysis over seven days, we found a rapid decrease in aggression within 24 hours of pair introduction in this highly territorial species. After this aggression reduction, the gradual increase in affiliative behaviors varied by type of affiliative behavior and ranged from one to seven days. We then measured neurobiological changes at three time points during this transition to uncover mechanisms that might govern this shift from aggressive to affiliative behavior, revealing novel sex differences that add to current research on biological mechanisms of social bonding. Specifically, we examined plasticity through mRNA expression of two perineuronal net (PNN) associated proteins, HAPLN and ACAN, in two brain regions implicated in affiliation, aggression, and social cognition: the ventral anterior cingulate cortex (vACC) and lateral septum (LS). The vACC in females exhibited higher expression levels of both of these PNN components relative to males. Additionally, we observed a decrease in ACAN mRNA expression in the vACC over the course of pair bond establishment, but no such change in the LS. Furthermore, oxytocin receptor (OXTR) and vasopressin receptor (AVPR) plasticity exhibited sex-specific patterns in the vACC during pair bond formation. Females displayed higher OXTR mRNA expression across the bonding period, whereas males expressed higher AVPR mRNA levels. In addition, our results uncovered a positive association between AVPR expression levels in the vACC and male-female nesting distance, a novel measure of affiliative behavior. We discuss how a decrease in PNNs could allow for an increase in receptor plasticity in the vACC as the pair bond is established. Moreover, we suggest that structural plasticity across this social transition may differ between males and females due to factors such as pre-pair sociality and aggression/territoriality changes. Plain English SummarySome mammals, such as the monogamous California mouse, establish a long term partner with which they defend territories, forage, and raise young. This is a large behavioral shift, wherein these animals form a cooperative dyad. In order to behaviorally adjust to this social change, we expected to see neural changes that are indicative of this adjustment, such as changes in neurons that make them more flexible or responsive to social stimuli. While we detected an increase in neural plasticity across the pair bond for both sexes, we also noted important sex differences in cortical regions that were not expected. The anterior cingulate cortex, which is conserved across mammals, is a brain area associated with social decision making and empathy. Sex differences in both receptors and plasticity were detected in this area, indicating that the sexes may use different neural mechanisms to adjust to large social changes. Further exploration into how the sexes use different modes of neural plasticity to appropriately adjust behavior is needed to explain this novel finding. HighlightsO_LICalifornia mice exhibited a graded shift from male-female aggression to greater affiliation across pair bond establishment. C_LIO_LIAggrecan mRNA expression, an indicator of perineuronal net (PNN) abundance, decreased in the ventral anterior cingulate cortex (vACC), but not the lateral septum (LS), across pair bond establishment. C_LIO_LIFemales displayed greater aggrecan mRNA in the vACC relative to males. C_LIO_LIThe vACC displayed greater oxytocin receptor (OXTR) mRNA expression in females and greater vasopressin receptor (AVPR) mRNA expression in males. C_LI

animal behavior and cognition↗

bioRxiv2022

Intranasal oxytocin enhances social preference for parents over peers in male but not female peri- adolescent California mice (Peromyscus californicus)

Peri-adolescence is a critical developmental stage marked by profound changes in the valence of social interactions with parents and peers. We hypothesized that the oxytocin (OXT) and vasopressin (AVP) systems, known for influencing social behavior, would be involved in the maintenance and breaking of bonding behavior expressed by peri-adolescent males and females. In rodents, OXT is associated with mother-pup bonding and may promote social attachment to members of the natal territory. AVP, on the other hand, can act in contrasting ways to OXT and has been associated with aggression and territoriality. Specifically, we predicted that in peri-adolescent male and female juveniles of the biparental and territorial California mouse (Peromyscus californicus), a) OXT would increase the social preferences for the parents over unfamiliar age-matched peers (one male and one female), and b) AVP would break the parent-offspring bond and either increase time in the neutral chamber and/or approach to their unfamiliar and novel peers. We examined anxiety and exploratory behavior using an elevated plus maze and a novel object task as a control. Peri-adolescent mice were administered an acute intranasal (IN) treatment of 0.5 IU/kg IN AVP, 0.5 IU/kg IN OXT, or saline control; five minutes later, the behavioral tests were conducted. As predicted, we found that IN OXT enhanced social preference for parents; however, this was only in male and not female peri-adolescent mice. IN AVP did not influence social preference in either sex. These effects appear specific to social behavior and not anxiety, as neither IN OXT nor AVP influenced behavior during the elevated plus maze or novel object tasks. To our knowledge, this is the first evidence indicating that OXT may play a role in promoting peri-adolescent social preferences for parents and delaying weaning in males. HIGHLIGHTSO_LIIn a 3-chambered choice test, peri-adolescent female and male California mice prefer their parents over peers or an empty chamber C_LIO_LIIntranasal oxytocin (IN OXT) enhances male but not female peri-adolescent social preference for their parents C_LIO_LIIntranasal arginine vasopressin (IN AVP) did not influence social preference in either sex C_LIO_LINeither IN OXT nor AVP alter peri-adolescent behavior in an elevated plus maze or novel object task C_LIO_LIOXT may play a role in delaying weaning in males C_LI

animal behavior and cognition↗

bioRxiv2021

Intranasal oxytocin reduces pre-courtship aggression and increases paternal response in California mice (Peromyscus californicus)

Oxytocin (OXT) is a neuropeptide that can facilitate prosocial behavior and decrease social stress and anxiety. We investigated whether acute pulses of intranasal (IN) OXT influenced social behavior during social challenges that are likely to occur throughout the lifespan of a wild mouse. To test this, we examined the acute effects of IN OXT in the male California mouse (Peromyscus californicus), a monogamous, biparental, and territorial rodent, using a within-subjects longitudinal design. Social challenges included a pre-courtship male-female encounter conducted during the initial aggressive and not the following affiliative phase of courtship, same-sex resident intruder test, and parental care test, with each test and dose separated by at least two weeks. Males were treated with intranasal infusions of 0.8 IU/kg OXT or saline controls 5-min before each behavioral test, receiving a total of three treatments of either IN OXT or saline control. We predicted that IN OXT would 1) decrease aggression and increase affiliation during the pre-courtship aggression phase, 2) increase aggression during resident intruder paradigms and 3) increase paternal care and vocalizations during a paternal care test. As predicted, during pre-courtship aggression with a novel female, IN OXT males displayed less contact aggression than control males, although with no change in affiliative behavior. However, post-pairing, during the resident intruder test, IN OXT males did not differ from control males in contact aggression. During the paternal care test, IN OXT males were quicker to approach their pups than control males but did not differ in vocalizations produced, unlike our previous research demonstrating an effect on vocalizations in females. In summary, during pre-courtship aggression and the paternal care test, IN OXT promoted prosocial approach; however, during the resident intruder test IN OXT did not alter social approach. These data suggest that IN OXT promotes prosocial approach specifically in social contexts that can lead to affiliation. HIGHLIGHTSO_LIIN OXT attenuates male aggression during pre-courtship encounters C_LIO_LIIN OXT does not attenuate male aggression during resident intruder encounters C_LIO_LIIN OXT increases paternal responsiveness during a paternal care challenge C_LIO_LIIN OXT in fathers does not influence total paternal care or vocalizations C_LI GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=52 SRC="FIGDIR/small/449160v1_ufig1.gif" ALT="Figure 1"> View larger version (12K): org.highwire.dtl.DTLVardef@63bf1corg.highwire.dtl.DTLVardef@97d8e7org.highwire.dtl.DTLVardef@12147d8org.highwire.dtl.DTLVardef@1f3f71c_HPS_FORMAT_FIGEXP M_FIG C_FIG

animal behavior and cognition↗

bioRxiv2021

Testosterone induces a conditioned place preference to the nest of a monogamous mouse under field conditions

Transient increases in testosterone (T-pulses) occur after social interactions in males of various vertebrate species, but the functions of T-pulses are poorly understood. Under laboratory conditions, the rewarding nature of T-pulses induces conditioned place preferences (CPPs), but what are the effects in a complex field environment? We present the first evidence that T-pulses administered to males at their nest site in the wild increased time spent at the nest regardless of pup presence in the monogamous, biparental, and territorial California mouse (Peromyscus californicus). Female partners of the T-males, in turn, spent less time at the nest. Independent of treatment, mice produced more ultrasonic vocalizations (USVs) when alone, but T-mice produced more USVs than controls. T-males produced USVs with a smaller bandwidth that likely traveled farther. Our combined results provide compelling evidence that T-pulses can significantly shift the behavioral focus and location of individuals in a complex field setting.

ecology↗

bioRxiv2020

An acute dose of intranasal oxytocin rapidly increases maternal communication and maintains maternal care in primiparous postpartum California mice

Maternal-offspring communication and care are essential for offspring survival. Oxytocin (OXT) is known for its role in initiation of maternal care, but whether OXT can rapidly influence maternal behavior or ultrasonic vocalizations (USVs; above 50 kHz) has not been examined. To test for rapid effects of OXT, California mouse mothers were administered an acute intranasal (IN) dose of OXT (0.8 IU/kg) followed by a separation test with three phases: habituation with pups in a new testing chamber, separation via a wire mesh, and finally reunion with pups. We measured maternal care, maternal USVs, and pup USVs. In mothers, we primarily observed simple sweep USVs, a short downward sweeping call around 50 kHz, and in pups we only observed pup whines, a long call with multiple harmonics ranging from 20 kHz to 50 kHz. We found that IN OXT rapidly and selectively enhanced the normal increase in maternal simple sweep USVs when mothers had physical access to pups (habituation and reunion), but not when mothers were physically separated from pups. Maternal-pup USVs were correlated upon reunion, but IN OXT did not influence this correlation. Finally, mothers given IN OXT showed a more positive change in retrievals/carrying and greater total maternal care upon reunion. Behavioral changes were specific to maternal behaviors (e.g. retrievals) as mothers given IN OXT did not differ from controls in stress-related behaviors (e.g. freezing). Overall, these findings highlight the rapid effects and context-dependent effect a single dose of IN OXT has on both maternal USV production and offspring care.

animal behavior and cognition↗

bioRxiv2020

Oxytocin promotes convergence in personality between members of a monogamous pair

Coordinated responses to challenge are essential to survival for bonded monogamous animals and may depend on behavioral compatibility. Oxytocin (OT) context-dependently regulates social affiliation and vocal communication, but its role in pair members decision to jointly respond to challenge is unclear. To test for OT effects, California mouse females received an intranasal dose of OT (IN-OT) or saline after bonding with males either matched or in their approach response to an aggressive vocal challenge. Pair mates were re-tested jointly for approach response, time spent together, and vocalizations. Females and males converged in their approach after pairing, but mismatched pairs with females given a single dose of IN-OT displayed a greater convergence that resulted from behavioral changes by both pair members. Unpaired females given IN-OT did not change their approach, indicating a social partner was necessary for effects to emerge. Moreover, IN-OT increased time spent approaching together, suggesting behavioral coordination beyond a further increase in bonding. This OT-induced increase in joint approach was associated with a decrease in the proportion of sustained vocalizations, a type of vocalization that can be associated with intra-pair conflict. Our results expand OTs effects on behavioral coordination and underscore the importance of emergent social context.

animal behavior and cognition↗