Oxytocin Release Increases With Age and Is Associated With Life Satisfaction and Prosocial Behaviors

 Publication: Nikola Benin, Ph.D

Paul J. Zak, Ben Curry, Tyler Owen, Jorge A. Barraza

Helping behaviors and life satisfaction generally increase after middle-age. Identifying the neural substrates of prosocial behaviors in older adults may offer additional insights into these changes over the lifespan. The present study examines the endogenous release of the neuromodulator oxytocin (OT) in participants aged 18–99 and its relationship to prosocial behaviors. OT has been shown to influence trust, altruism, charity, and generosity, yet the effect of age on OT release has not been well-established. Blood samples before and after a video stimulus were obtained from 103 participants in order to examine the impact of OT on prosocial behaviors. We found that OT release following a social prime increased with age (r = 0.49, p = 0.001) and that OT moderated the relationship between age and donations to charity. We tested for robustness by examining three additional prosocial behaviors, money and goods donated to charity during the past year and social-sector volunteering. OT moderated the impact of age on all three prosocial behaviors (ps < 0.05). The analysis also showed that participants’ change in OT was positively associated with satisfaction with life (p = 0.04), empathic concern (p = 0.015), dispositional gratitude (p = 0.019), and religious commitment (p = 0.001). Our findings indicate that the neural chemistry that helps sustain social relationships and live a fulfilled life appear to strengthen with age.

Introduction

The physical effects of aging on the body have been well documented (Saxon et al., 2014). Similarly, the effect of aging on cognitive function has been extensively studied (Meaney et al., 1995; Conrad and Bimonte-Nelson, 2010). For example, aging impairs efficiency and processing speed (Salthouse, 1994, 1996; Li et al., 2004), explicit learning (Salthouse, 2006), working memory (Salthouse, 1992; McArdle et al., 2004), and attention and problem-solving (Craik and Salthouse, 2000). These changes may result from the reduction of gray matter volume in brain regions as one ages (Brown and Ridderinkhof, 2009), including the anterior cingulate cortex, the orbital frontal cortex, the superior temporal sulcus, the insula, and the dorsal and ventral striatum (Matochik et al., 2000; Raz et al., 2000; Good et al., 2001; Sowell et al., 2003; Allen et al., 2005; Walhovd et al., 2005).

Social behaviors and emotional responses also change with age (Midlarsky et al., 2015; Matsumoto et al., 2016; Pornpattananangkul et al., 2019). Seniors spend more time volunteering and donate a larger proportion of their income to charity compared to younger adults (Simmons and Emanuele, 2004; Omoto et al., 2009; Choi and Chou, 2010; Bekkers and Wiepking, 2011; Wiles and Jayasinha, 2013). Both of these effects are stronger for religiously active older adults (Lee and Chang, 2007; Bekkers and Wiepking, 2011). In laboratory studies, seniors share more money with strangers than younger adults (Beadle et al., 2015) with and without empathy priming (Matsumoto et al., 2016; Rosen et al., 2016; Rosi et al., 2019).

A number of factors are associated with increased prosociality in seniors compared to younger cohorts. These include increased positive affect (Stanley and Isaacowitz, 2011), the use of intuition rather than calculation during decisions (Rosi et al., 2019), and improved emotional regulation (Larcom and Isaacowitz, 2009; Charles and Carstensen, 2010; Samanez-Larkin and Carstensen, 2011). Older adults may develop skills that improve their moods that younger people are less likely to use such as gazing at happy faces (Isaacowitz et al., 2009) though there is significant variation across individuals (Stanley and Isaacowitz, 2012). Age-related positivity also manifests in older adults as they attend to positive information more than negative information (Reed and Carstensen, 2012). Older adults are also better at reasoning about interpersonal and intergroup conflicts (Artistico et al., 2003; Thornton and Dumke, 2005; Grossmann et al., 2010), and have more accurate evaluations of their own knowledge (Kovalchik et al., 2005). Prosocial behaviors in seniors, relative to younger people, may be more likely to arise because of heightened state-induced affective empathy (Ze et al., 2014; Rosen et al., 2016; Sun et al., 2018; Bailey et al., 2021). Yet, no differences are found in trait empathy between older and younger adults (Konrath et al., 2011; O’Brien et al., 2013; Sun et al., 2018).

Age-varying neurochemical responses might help explain seniors’ prosociality. Correlational and experimental studies of prosocial behaviors suggest oxytocin (OT) as a likely candidate. The release of OT is associated with empathic concern (Barraza and Zak, 2009, 2013) while synthetic OT administration enhances empathy (Hurlemann et al., 2010; Shamay-Tsoory et al., 2013). Both the change in endogenous OT and synthetic OT administration have been associated with donations to charity (Barraza and Zak, 2009; Barraza et al., 2011), generosity toward strangers (Zak et al., 2007; Pornpattananangkul et al., 2017), and trustworthiness (Zak et al., 2004, 2005; Terris et al., 2018) among other prosocial behaviors (Barraza and Zak, 2013) though generosity after OT administration may be biased toward in-groups (Ten Velden et al., 2017) and OT administration may or may not affect trust (Kosfeld et al., 2005; Declerck et al., 2020). In addition, the effect of OT infusion on recognizing emotions in faces shows a positive age gradient (Campbell et al., 2014; Ebner et al., 2015a,b; Horta et al., 2019).

Evidence for the effect of OT on social-emotional responses in older adults comes primarily from intranasal OT administration studies, albeit with mixed findings (Horta et al., 2020). For instance, single-dose OT administration improves emotional recognition in healthy older men (Campbell et al., 2014) and in dementia patients (Jesso et al., 2011). However, replication using a larger sample and additional emotional recognition tasks failed to replicate this finding (Grainger et al., 2018) and two meta analyses show variable effects (Shahrestani et al., 2013; Leppanen et al., 2017). OT administration improves self-reported mood (Ebner et al., 2015a,b) and enhances resting state amygdala-mPFC coupling (Ebner et al., 2013) in older men but not older women. A three-dose OT administration study in a sample of older adults with dementia demonstrated reduced apathy, increased expressions of empathy, and improved caregiver interactions (Finger et al., 2015). A longer (10-day) trial of intranasal OT administration in healthy older adults (mean 80 years) revealed improved dispositional gratitude and reduced fatigue (Barraza et al., 2013).

While synthetic OT administration in older adults may have clinical value, such an intervention may be premature until endogenous OT release in seniors is understood. Some reports find basal OT declines with age with a larger effect for women compared to men (Plasencia et al., 2019), although the opposite effect has also been reported (Kunitake et al., 2020). The current study measures OT reactivity in response to a video stimulus with social content because it is the release of OT that has been associated with prosocial behaviors and the quality of relationships (Zak, 2012). Basal OT is generally unpredictive of behavior in healthy adults (Cochran et al., 2013). The reactivity of peripheral OT to social stimuli occurs within 1 s of stimulus onset and reflects a change in central OT via hypothalamic control (Valstad et al., 2017). The correspondence between the change in central and peripheral OT is the reason why a change in OT measured in blood is related to behaviors (Zak et al., 2004, 2005; Zak, 2012; Barraza and Zak, 2013; Terris et al., 2018). Of interest for the present study, OT-expressing neurons appear to be unaffected by age (Wierda et al., 1991; Ishunina et al., 1999) suggesting that OT is a feasible candidate to influence the age gradient in prosociality.

If OT release in seniors is greater than that in younger adults and is associated with prosociality, it may also be related to the age gradient in satisfaction with life (SWL). Many, though not all, studies report that SWL rises after middle-age and stays high until an advanced age (Diener and Suh, 1997; Diener, 2009; Hansen and Slagsvold, 2012; Jivraj et al., 2014). Part of this effect is due to improved coping skills in the face of stress (Hamarat et al., 2002). More generally, life satisfaction among seniors covaries with health, marital status, religiosity, and cognitive function (Bergan and McConatha, 2001; Bailey and Snyder, 2007; Parra-Rizo and Sanchis-Soler, 2020). Basal OT has been associated with higher SWL in young adults (Garforth et al., 2020) but has not to date been examined in older populations.

The study reported here was designed to test the hypothesis that socially primed OT release will increase with age. We also hypothesized that the increase in OT will positively correlate with changes in age-related prosocial behaviors as well as with participants’ SWL. These three hypotheses seek to shed light on the neural mechanisms that influence social behaviors of older adults compared to younger ones.