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Acute social isolation evokes midbrain craving responses similar to hunger.

ABSTRACT: When people are forced to be isolated from each other, do they crave social interactions? To address this question, we used functional magnetic resonance imaging to measure neural responses evoked by food and social cues after participants (n = 40) experienced 10 h of mandated fasting or total social isolation. After isolation, people felt lonely and craved social interaction. Midbrain regions showed selective activation to food cues after fasting and to social cues after isolation; these responses were correlated with self-reported craving. By contrast, striatal and cortical regions differentiated between craving food and craving social interaction. Across deprivation sessions, we found that deprivation narrows and focuses the brain's motivational responses to the deprived target. Our results support the intuitive idea that acute isolation causes social craving, similar to the way fasting causes hunger.

SUBMITTER: Tomova L

PROVIDER: S-EPMC8580014 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Acute social isolation evokes midbrain craving responses similar to hunger.

Tomova Livia L Wang Kimberly L KL Thompson Todd T Matthews Gillian A GA Takahashi Atsushi A Tye Kay M KM Saxe Rebecca R

Nature neuroscience 20201123 12

When people are forced to be isolated from each other, do they crave social interactions? To address this question, we used functional magnetic resonance imaging to measure neural responses evoked by food and social cues after participants (n = 40) experienced 10 h of mandated fasting or total social isolation. After isolation, people felt lonely and craved social interaction. Midbrain regions showed selective activation to food cues after fasting and to social cues after isolation; these respon ...[more]

PMID: 33230328

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Project description:BackgroundSocial interaction is crucial for mental health across animal species. Social experiences, especially in early-life stages, strongly influence brain function and social behavior later in life. Acute social isolation (SI) increases motivation to seek social interaction, but little is known about its underlying neuronal and circuitry mechanisms. Here, we focus on oxytocin signaling in the ventral tegmental area (VTA), a vital node of the brain's reward network, as a potential mechanism for SI-induced craving for social interaction.MethodsAdolescent (4-week-old) or adult (14-week-old) male C57BL/6J mice underwent a 1-week SI. Free interaction, object exploration, three-chamber social approach, and habituation tests were used to assess social and non-social behavior changes. Viral vectors were used to decipher the underlying neural circuitry, and chemogenetic techniques were applied to modify neuronal activity.ResultsWe found that in male C57BL/6J mice, SI during adolescence, but not adulthood, leads to increased craving for social interaction and object exploration, accompanied by impaired social habituation, social novelty preference, and social recognition memory (SRM). SI-induced craving for social interaction and SRM deficit is still observed upon regrouping. Through cell-type-specific manipulations with designer receptors exclusively activated by designer drugs (DREADD), we show that oxytocin neurons in the paraventricular nucleus of the hypothalamus (PVN) are crucial for SI-induced social behavior changes. Chemogenetic activation of PVN oxytocin neurons recapitulates social behavior changes observed in SI mice, whereas chemogenetic inhibition of oxytocin neurons prevents social behavior changes caused by SI. Moreover, we found that dopaminergic neurons in the VTA mediate SI-induced craving for social interaction through their projections to the medial prefrontal cortex (mPFC), but not to the nucleus accumbens. Injection of a specific oxytocin receptor antagonist L368,899 into the VTA or chemical lesions of dopaminergic axon terminals in the mPFC with local application of 6-hydroxydopamine ameliorates SI-induced social behavior changes.ConclusionsThese findings suggest that adolescent SI has enduring effects on social behaviors in male mice through an oxytocinergic modulation of the VTA-to-mPFC dopaminergic circuit activity.

Project description:BackgroundEating plays an important role in mental and physical health and is influenced by affective (e.g., emotions, stress) and appetitive (i.e., food craving, hunger) states, among others. Yet, substantial temporal variability and marked individual differences in these relationships have been reported. Exploratory data analytical approaches that account for variability between and within individuals might benefit respective theory development and subsequent confirmatory studies.MethodsAcross 2 weeks, 115 individuals (83% female) reported on momentary affective states, hunger, and food craving six times a day. Based on these ecological momentary assessment (EMA) data we investigated whether latent class vector-autoregression (LCVAR) can identify different clusters of participants based on similarities in their temporal associations between these states.ResultsLCVAR allocated participants into three distinct clusters. Within clusters, we found both positive and negative associations between affective states and hunger/food craving, which further varied temporally across lags. Associations between hunger/food craving and subsequent affective states were more pronounced than vice versa. Clusters differed on eating-related traits such as stress-eating and food craving as well as on EMA completion rates.DiscussionLCVAR provides novel opportunities to analyse time-series data in affective science and eating behaviour research and uncovers that traditional models of affect-eating relationships might be overly simplistic. Temporal associations differ between subgroups of individuals with specific links to eating-related traits. Moreover, even within subgroups, differences in associations across time and specific affective states can be observed. To account for this high degree of variability, future research and theories should consider individual differences in direction and time lag of associations between affective states and eating behaviour, daytime and specific affective states. In addition to that, methodological implications for EMA research are discussed.

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Acute social isolation evokes midbrain craving responses similar to hunger.

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Acute social isolation evokes midbrain craving responses similar to hunger.

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