Journal Identification = NRP Article Identification = 0598 Date: June 21, 2021 Time: 1:43 pm
doi:10.1684/nrp.2020.0598
REVUE DE NEUROPSYCHOLOGIE
NEUROSCIENCES COGNITIVES ET CLINIQUES
87
Point of view
Rev Neuropsychol
2020 ; 12 (S1) : 87-8
On lockdown: Social homeostasis or the
rewarding nature of social contact * À propos du confinement :
l’homéostasie sociale ou la nature gratifiante du contact social
Robert Jaffard INCIA, UMR CNRS 5287, University of Bordeaux
<robert.jaffard@icloud.com>
To cite this article: Jaffard R. On lock- down: Social homeostasis or the rewarding nature of social contact.
Rev Neuropsychol 2020;12(S1):87-8 doi:10.1684/nrp.2020.0598
S
ocial contact is a fundamental need of man and non-human social species. Social life offers increased security and chances of survival, including protection from predators, food gathering, reproduction and care of offspring, and social learning. Research in recent decades has analyzed the positive physiological, neurobiological and behavioral consequences of social ties and contacts, as opposed to the negative consequences of isolation (objec- tive) and “loneliness” (subjective). To give just one example, close and enduring bonds between female baboons are a guarantee of longevity for them and their offspring, an effect that seems to be linked to a reduction in stress. More gener- ally, even in the absence of external threats to survival, the permanence of social contact is associated with increased longevity in many social species, including insects.However, in these times of lockdown, the purpose of this note is rather to analyse social contacts as a “need” or social motivation to avoid the negative or aversive conse- quences of isolation and, moreover, to examine the neural mechanisms involved. It will be seen that most of our cur- rent knowledge, much of it recent, comes from studies in rodents (mice, rats and monogamous voles).
Behavioral effects of acute social isolation
In many animals, a period of “forced” social isolation, even a short one (a few hours), increases the motivation to “find”−and interact with−congeners, whereas chronic isolation (several days) leads to depressive and anxious type behaviors and may lead to increased aggressive behavior.
Experimentally, rodents briefly deprived of social contact, learn to press a lever or run through a maze to access a congener. In some situations, they are also able to release
∗This article is an English language translation of the following article:
Jaffard R. À propos du confinement : l’homéostasie sociale ou la nature gratifiante du contact social.Rev Neuropsychol2020 ; 12 (2) : 210-2.
doi:10.1684/nrp.2020.0573.
Correspondence:
R. Jaffard
a cagemate locked in a box or help it out of a water- filled pool area, a behavior that may be empathetic in response to distress or simply motivated by the need for social contact. Either way, these prosocial behaviors are selective and highly motivated.
For example, it has recently been shown that in situ- ations of choice, male or female rats prefer social reward (congeneric) over the “compulsive” self-administration of a drug such as heroin or methamphetamine. Finally, brief isolation is sufficient to increase the time spent in regions previously associated with social contact (i.e., conditioned place preference), a result similar to that observed for a place that contained food, allowed drug self-administration or intracranial stimulation of the brain reward system. Taken together, these results suggest that a “social deficit” leads to the onset of social motivation comparable to hunger or other types of motivation.
The social homeostasis system
1The current hypothesis posits the existence of a sys- tem of social homeostasis where the detection of a deficit of social contact in relation to a state of equilibrium (“set point”), would generate the motivational impulse intended, viathe behavioral effector, to restore these contacts, thus guaranteeing optimal conditions of existence and survival.
Such a system is conceptually analogous to the homeosta- sis mechanisms which, starting from a specific motivation (hunger, thirst) and a specific oriented behavior, lead to the correction of a physiological (respectively energetic or hydromineral) imbalance. Nevertheless, the identity, func- tioning and coordination of the neural circuits underlying the detection and evaluation of social connection deficits and the activation of the effector systems intended to com- pensate for them remain largely unknown.
1 The concept of homeostasis refers to the capacity, present in all liv- ing organisms, to keep permanently certain functional variables within limits compatible with survival. The term social homeostasis was first used to account for the maintenance of a stable organization within colonies of social insects (ants) assimilated to superorganisms.
Journal Identification = NRP Article Identification = 0598 Date: June 21, 2021 Time: 1:43 pm
REVUE DE NEUROPSYCHOLOGIE
NEUROSCIENCES COGNITIVES ET CLINIQUES
88
Point of view
Neural mechanisms of social homeostasis
The search for social contact triggered by isolation is directed by two motivations of opposing valence: an aver- sive (negative) motivation to avoid this isolation and a (positive) motivation to approach the social reward. Recent work on various components of the rodent mesocorticol- imbic dopaminergic (DA) system has made it possible to dissociate these two components[1].
On the one hand, DA neurons originating from the ven- tral tegmental area (VTA) and projecting onto the nucleus accumbens (NAcc) have a major role in the hedonic value of social interaction and also involve oxytocin activity. It is furthermore established that if the VTA-NAcc reward system underlies a very wide spectrum of “positively” motivated behaviors (food, sex, addictive drugs...), oxytocin (a neu- ropeptide known as the “social bond” neuropeptide) only influences the social forms of these behaviors, such as the social affiliation of the biparental monogamous vole.
On the other hand, the DA neurons of the dorsal raphe nucleus (DRN) are involved in the negative (or aversive) affective state induced by a short social isolation lead- ing, through its “avoidance”, to a re-engagement in social contacts.
It is important to emphasize that the data, summarized here in a very succinct way, establish the necessary and sufficient character of the reported mechanisms (by opto- genetic control of identified neurons) as well as their social specificity (through the use of choice situations).
From animal to man
Work in humans has analyzed the behavioral and, to a lesser extent, neural consequences of “social rejection” or a “feeling of loneliness”. The different situations of social rejection are above all marked by “negative emotions” that can lead to alternative affiliation efforts but also to antisocial avoidance behaviors. At the same time, social rejection is accompanied by an activation of brain regions associated with aversive states −including physical pain− which is reminiscent of the aversive component generated by iso- lation in rodents (above).
The chronic feeling of loneliness, which most often reduces the desire for social connection, has however been associated with an activation (fMRI) of the NAcc to the presentation of pictures of close (but not stanger) people, somewhat reminiscent of the results obtained in rats (above).
But a major caveat of research on loneliness is its corre-
lational nature. For example, is it loneliness that reduces motivation for social contact or the opposite?. Only experi- mental approaches to induced acute social isolation, similar to those carried out in rodents, can answer this question.
Now, a few months ago, an MIT team deposited in
“BioRvix” a pre-publication in which 40 participants with a
“normal” social life were subjected to a 10-hour “objective”
isolation [2]. The results showed that this acute isolation induced an explicit increase in the desire for social contact but also an aversion to the isolation suffered (feeling of dis- comfort, reduction in the feeling of “happiness”). The fMRI data also showed that it selectively increases the responses of the VTA and the substantia nigra (SN)−components of the dopaminergic “reward system” of the midbrain−to images of social interactions (e.g. discussions between individu- als). In addition, VTA/SN responses were greater in subjects who had a greater need for social contact. Finally, the level of activation was also proportional to the richness of sub- jects’ pre-existing social relationships, and thus, possibly, to their personal social “set point”. Note that this experiment also reported similar results, but after a 10-hour of fasting that provoked a selective response of the same brain regions (VTA/SN) to the presentation, this time, of food cues. In sum, in the same subjects, the same mesencephalic regions were activated by social cues after a social (but not food) “fast”
and by food cues after a food (but not social) fast.
Conclusion
Of course, all this data raises some questions.
The first concerns the selectivity of the effects of social isolation in rodents. Results show that these effects can extend to other motivations such as food, alcohol or mor- phine. It is possible that this extended impact is related to the long duration of isolation leading to several compensations and to the suppression of the motivation for social contact.
The second relates to the nature of social isolation which, even if “objective”, is probably not “perceived” or
“felt” in the same way in animals −where it is mainly sensory− and in humans where it has a marked subjec- tive component. In addition, there are important anatomical differences between the dopaminergic reward circuits of humans and rodents. These discrepancies question the rel- evance of translational research aimed at correcting social motivation disorders such as autism or social phobia.
Conflicts of interest none
References
1.Matthews GA, Tye KM. Neural mechanisms of social homeostasis.
Ann NY Acad Sci2019 ; 1457 : 5-25.
2.Tomova L, Wang K, Thompson T, et al. The need to con- nect: acute social isolation causes neural craving responses similar to hunger. BioRvix 2020. https://www.biorxiv.org/content/10.1101/
2020.03.25.006643v2.
