Effects of social disconnection on reward processing: Longitudinal measures across adolescence
Creators: name: Li, Jie Lin
name: Bignardi, Giacomo
name: Blakemore, Sarah-Jayne
name: Tomova, Livia
Publisher: name: OSF Registries
Year: 2024
Subjects: subject: Medicine and Health Sciences
subject: Social and Behavioral Sciences
subject: adolescence
subject: fMRI
subject: loneliness
subject: reward
subject: social disconnection

description: Social connection is central for health and well-being in humans. Feeling socially connected can help improve cancer survival (Costanzo et al., 2005), cardiovascular health (Rutledge et al., 2004) and mental health (Sintonen &amp; Pehkonen, 2014). Chronic social disconnection, in contrast, is associated with profound negative effects on physical and mental health (Hawkley &amp; Cacioppo, 2010), even leading to increased mortality (Wang et al., 2023). 

The umbrella term social connection encompasses the number/frequency of social connections, the amount of social support and whether relationships are personally satisfying (Holt-Lunstad, 2021). Social connection exists on a continuum ranging from highly connected to highly disconnected and involves objective elements (e.g., number of friends) and subjective elements (e.g., loneliness, defined as a subjective lack of social connection (J. T. Cacioppo &amp; Cacioppo, 2014). These are typically interrelated but can also be independent. For example, people can feel lonely in a crowd (J. T. Cacioppo et al., 2009).

Social connection is especially important during the formative period of adolescence (defined as 10-24 years; (Sawyer et al., 2018; Tomova et al., 2021). Adolescence is a particularly sensitive period for development of higher-level cognitive functions and social skills (Blakemore, 2008; Dumontheil et al., 2010; Kilford et al., 2016). Indeed, the “social brain” (the network of brain regions involved in social cognition) undergoes significant development during adolescence (Blakemore, 2008) and adolescents can be hypersensitive to social stimuli, both positive and negative (Foulkes &amp; Blakemore, 2016), and particularly to social exclusion (Mills et al., 2014). This highlights the importance of social interactions for healthy adolescent development. However, loneliness has increased in adolescents over the past decade (Cigna, 2018; Twenge et al., 2021; Yang &amp; Victor, 2011).

Thus, an urgent question is how a lack of social connection affects outcomes during this sensitive period of development. 

Many brain areas undergo substantial development during adolescence. As well as the social brain, another neural circuit that undergoes development during adolescence and may be impacted by social connection is the reward system. Subcortical regions functionally associated with reward processing undergo considerable changes and reorganisation during adolescence (Walker et al., 2017). Studies in animal models have shown that social isolation during adolescence negatively impacts brain development, leading to effects resembling features of human neuropsychiatric disorders (Orben et al., 2020). These studies have shown that social isolation during adolescence impacts processing in the reward circuit and increases reward sensitivity (leading to increased reward seeking and proneness to develop addictions; Burke et al., 2017; Hall, 1998). However, it remains unclear how well these results translate to humans.

Human studies on the effects of social disconnection are mainly cross-sectional and correlational, leaving the direction of influence unclear. Only a small number of longitudinal studies have investigated how the experience of loneliness (i.e., the subjective experience of perceived isolation(J. T. Cacioppo &amp; Hawkley, 2009)) during adolescence impacts emotions and cognition. An advantage of longitudinal research is that between- and within-subjects effects of loneliness can be disentangled. For example, within-subject effects of fluctuations in an individual’s loneliness over time, relative to their average loneliness levels, can be related to fluctuations in other outcomes. When analysed appropriately, these within-subject associations control for time-invariant confounders that are stable over the study period (e.g., ethnicity, parental SES) and thus provide improved causal estimates (Murayama &amp; Gfrörer, 2022) . 

Most existing longitudinal work has focused on the effects of loneliness on mental health. For example, adolescent loneliness measured at ages 11- 20 was linked to higher odds of reporting depression seven years later (ages 18-27 years; (Goosby et al., 2013)). Participants grouped into the ‘stable high’ or ‘moderate increasing’ trajectories of loneliness had higher depression scores at age 17 than participants grouped into ‘stable low’ or ‘moderate decreasing’ trajectories (Qualter et al., 2013). Similarly, Ladd and Ettekal (2013) aimed to identify trajectories of loneliness and depression scores during adolescence and found that loneliness and depression trajectories correlated positively (Ladd &amp; Ettekal, 2013a). Prinstein and La Greca (2002), who implemented a longitudinal design with two time points (T1= grades 4–6 and T2= grades 10–12), reported bivariate correlations indicating time 1 depressive symptoms were significantly related to time 2 loneliness and time 1 loneliness was significantly related to time 2 depressive symptoms (Prinstein &amp; La Greca, 2002b). In sum, the findings from longitudinal studies to date suggest there might be a reciprocal relationship between depression and loneliness.

Research on the effects of social disconnection on the reward system in humans is scarce. A recent behavioural study using an experimental approach in human adolescents showed increased reward responsiveness following short-term isolation in humans (Tomova, 2022), in line with animal findings. While these results suggest that the effects of isolation on the reward system might be similar across species, it is important to note that isolation not only impacts subjective feelings of connectedness (such as feelings of state loneliness) but also other processes such as mood, boredom and general arousal. Thus, it remains unclear whether real-life feelings of social disconnection result in similar effects on the reward system as observed in experimental isolation studies.

The present study aims to assess this question by using longitudinal data from the ABCD study (https://abcdstudy.org/) to assess whether: i) within-subject changes in social disconnection over time predict within-subject changes in neural correlates and questionnaire measures of reward responsiveness; and ii) between-subjects differences in social disconnection predict between-subjects differences in neural correlates and questionnaire measures of reward responsiveness in adolescents. Data from the ABCD study collected at ages 9-10, 11-12 and 13-14 years will be analysed.

Social disconnection will be assessed using three different scales related to social interactions within ABCD (see Analysis Plan for details) measuring number of friends, perceived social support and parent-reported loneliness. 

Reward responsiveness will be assessed using functional magnetic resonance imaging (fMRI) measures of reward anticipation in the Monetary Incentive Delay (MID) task. We will focus only on the anticipation phase and not the outcome phase of the task for methodological reasons (see (Demidenko et al., 2021) for details).

We will also run secondary analyses using questionnaire measures of the ABCD Youth Behavioral Inhibition/Behavioral Approach System (BIS/BAS) Scales BAS subscale as a measure of self-reported reward responsiveness.