Effects of aggressive temperament on endogenous oxytocin levels in adult titi monkeys

Abstract

Coordination of oxytocin (OT) activity and partner interactions is important for the facilitation and maintenance of monogamous pair bonds. We used coppery titi monkeys (Callicebus cupreus) to identify the effects of male aggressive temperament on OT activity, affiliative partner-directed behaviors, aggressive partner-directed behaviors, anxiety-related behaviors, and hormone-behavior interactions. We used a mirror technique, simulating an intruder in the home territory of pairs to elicit behavioral responses, and quantified behaviors using an established ethogram. Plasma concentrations of OT (pg/ml) were quantified using enzyme immunoassay. We used general linear mixed models to predict 1) percent change in OT as a function of aggression score, and 2) percent change in behaviors as a function of aggression, OT, and OT by aggression interactions. High-aggressive males exhibited a significant drop in OT concentration relative to control when exposed to the front of the mirror (β = -0.22, SE = 0.10, t = -2.20, p = 0.04). High-aggressive males spent significantly less time in contact with their mates (β = -1.35, SE = 0.60, t = -2.26, p = 0.04) and lip-smacked less (β = -1.02, SE = 0.44, t = -2.32, p = 0.03) relative to control. We also saw a trend toward an interaction effect between OT and proximity such that High-aggressive males displaying a drop in OT exhibited a smaller percent increase in social proximity (β = 6.80, SE = 3.48, t = 1.96, p = 0.07). Males exhibiting a decrease in OT also trended toward back-arching and tail-lashing less in response to the mirror (β = 4.53, SE = 2.5, t = 1.82, p = 0.09). To our knowledge, this is the first empirical study to examine interactions between OT and temperament in adult monogamous primates. Future studies should incorporate measures of pair-mate interactions and early-life experience to further understand variation in responses to social stressors and their effects on pair bonding.

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

“…Studies in humans have also shown an association between increased aggression, competition, and OXT (DeWall et al, 2014; Ne’eman et al, 2016; De Dreu, 2012; Fischer-Shofty et al, 2013). However, studies in monogamous marmosets (Cavanaugh et al, 2018), monogamous titi monkeys (Witczak et al, 2018), female and male rats (De Jong et al, 2014; Calcagnoli et al, 2013; Calcagnoli et al, 2015a; Calcagnoli et al, 2015b), house mice primed for aggressive behavior due to social isolation (Tan et al, 2019), and house mice bred for callous traits (Zoratto et al, 2018) found that OXT was associated with reduced intrasexual competition and aggression. Together with our data, these findings suggest that OXT’s effect on intrasexual aggression may depend heavily on the species, brain areas activated by OXT, and social context.…”

The neural circuits of monogamous behavior

“…Accordingly, differences in levels of estrogen-receptor α (ERα) expression in the MeA, mPOA, and the VMN are also associated with monogamous behavior and parental care in mandarin voles (Wu et al, 2011). (Aragona et al, 2003;Gingrich et al, 2005), d (López-Gutiérrez et al, 2021, e (Aragona et al, 2006), f (Bales et al, 2007), g (Maninger et al, 2017b), h (Arias Del Razo et al, 2020), i (Hostetler et al, 2017), by D1 receptor antagonist [11C]-SCH2339 binding detection, j (Maninger et al, 2017b), k (Burkett et al, 2011;Resendez et al, 2013Resendez et al, , 2016; l (Lei et al, 2010), m (Lambert et al, 2021), n (Gossman et al, 2021), o (King et al, 2016), p (Ophir et al, 2008b), q (Liu et al, 2001;), r (Pitkow et al, 2001;), s (Witczak et al, 2018), t (Cavanaugh et al, 2014(Cavanaugh et al, , 2018a With respect to OT variants and their impact on behavior, interesting discoveries have been made. Phylogenetic evidence has shown not only OT genetic sequence differences across closely related species, but also a functional cross-talk between AVP and OT, and structural variations in the expressed nonapeptides that could subsequently impact their involvement in neural circuits (French et al, 2016;Pierce et al, 2020).…”

“…VTA, ventral tegmental area. a ( Lim and Young, 2004 ), b ( Amadei et al, 2017 ), c ( Aragona et al, 2003 ; Gingrich et al, 2005 ), d ( López-Gutiérrez et al, 2021 ), e ( Aragona et al, 2006 ), f ( Bales et al, 2007 ), g ( Maninger et al, 2017b ), h ( Arias Del Razo et al, 2020 ), i ( Hostetler et al, 2017 ), by D1 receptor antagonist [11C]-SCH2339 binding detection, j ( Maninger et al, 2017b ), k ( Burkett et al, 2011 ; Resendez et al, 2013 , 2016 ); l ( Lei et al, 2010 ), m ( Lambert et al, 2021 ), n ( Gossman et al, 2021 ), o ( King et al, 2016 ), p ( Ophir et al, 2008b ), q ( Liu et al, 2001 ; Lim and Young, 2004 ), r ( Pitkow et al, 2001 ; Lim and Young, 2004 ), s ( Witczak et al, 2018 ), t ( Cavanaugh et al, 2014 , 2018a ), u ( Rothwell et al, 2019 ), v ( Ragen et al, 2015b ), w ( Carp et al, 2019 ), x ( Jarcho et al, 2011 ), y ( Cavanaugh et al, 2018b ), z ( Baxter et al, 2020 )), a+ ( Borie et al, 2022 ), b+ ( Cushing et al, 2003 ), c+ ( Lei et al, 2017 ), d+ ( Jia et al, 2008 ), e+ ( He et al, 2013 ), f+ ( An et al, 2013 ).…”

An Animal Model for Mammalian Attachment: Infant Titi Monkey (Plecturocebus cupreus) Attachment Behavior Is Associated With Their Social Behavior as Adults

“…For example, individual variation in aggression has been shown to predict affiliation within a pair. More characteristically aggressive males (which show higher levels of mate-guarding or "jealous" behavior) tended to be less affiliative with their partners (Witczak et al, 2018).…”