Incarcerated individuals: Stronger associations for disinhibition with substance use problems, self-harm, and staff ratings of prison misbehavior among females compared to males

Testing for Sex Differences in the Nomological Network of the Triarchic Model of Psychopathy in Incarcerated Individuals. Claudio Sica, Emily R. Perkins, Keanan J. Joyner, Corrado Caudek, Gioia Bottesi, Maria Caruso, Paolo Giulini, Marta Ghisi & Christopher J. Patrick. Journal of Psychopathology and Behavioral Assessment, Jul 16 2021. https://link.springer.com/article/10.1007/s10862-021-09897-w

Abstract: The triarchic model of psychopathy conceptualizes variants of this clinical condition as expressions of three distinct biobehavioral dispositions, termed boldness, meanness, and disinhibition. As a trait-oriented model, the triarchic model situates psychopathy within a broader nomological network of personality and psychopathology, and has proven useful for characterizing how psychopathy relates to variables in these domains as well as to biological and behavioral variables. The current study was the first to examine sex differences in the external correlates of psychopathic traits as described by the triarchic model in a prison sample. Results were generally consistent with hypotheses: The triarchic traits related to measures of personality and psychopathology in patterns that were largely consistent across sex, but with some notable differences between males and females, in the correlates of disinhibition in particular. These included stronger associations for disinhibition with substance use problems, self-harm, and staff ratings of prison misbehavior among females compared to males. Findings from this study support the value of the triarchic model for understanding similarities and differences in the nomological network of psychopathy in incarcerated males and females.

Discussion

This study sought to elucidate sex differences in the nomological network of the triarchic model of psychopathy among incarcerated individuals, adding to scientific understanding about the model’s external validity. Findings generally complement and extend prior work comparing males and females in non-incarcerated populations and overcome an important limitation of the existing literature: a reliance on the PCL-R and related measures, which emphasize crime-related aspects of psychopathy to the exclusion of adaptive features. The triarchic model of psychopathy is designed to capture dispositional characteristics that may be expressed in a variety of phenotypes, including engagement in crime. The current study examined other manifestations of the triarchic traits — i.e., patterns of relations to other relevant constructs, such as personality and psychopathology — within a sample characterized by elevated engagement in crime, as well as investigating sex differences in these patterns.

The Triarchic Model in a Prison Sample

The current results advance scientific understanding of the triarchic model in a prison sample. Broadly, findings were consistent with hypotheses based on previous studies. Consistent with the theoretical conceptualization of boldness and with prior research (e.g., Sica et al., 2015), we found in this mixed-sex prison sample that TriPM Boldness was negatively associated with certain maladaptive constructs such as neuroticism and hopelessness, suggesting it adequately represents some aspects of psychological resilience against distress in an incarcerated sample (see Gottfried et al., 2019). Interestingly, and contrary to hypotheses, boldness was unrelated to self-harm in this sample; it may that this trait is less closely tied to behavioral expressions of distress than to the psychological experience itself. Importantly, despite its generally negative relations with distress measures, boldness was predictive of greater substance use problems and lower staff ratings of prison behavior and reintegration prognosis following release. These results are in line with other findings suggesting that boldness does not merely index positive adjustment (Lilienfeld et al., 2012, 2018; cf. Miller & Lynam, 2012). Multiple studies have found positive associations between boldness and various forms of maladaptive behavior (e.g., Anestis et al., 2018; Baroncelli et al., in press; Coffey et al., 2018; Hicks et al., 2014), including in prison samples (Sellbom et al., 2018). Notably, however, a previous study of incarcerated males found boldness to be associated with lower structured clinical judgments of risk for future violence (Sellbom et al., 2018), in contrast to the present results regarding current prison behavior and reintegration prognosis. Further research is needed to understand boldness and behavior in correctional settings.

Relations between TriPM Meanness and FFM traits were generally consistent with expectations, particularly the strong negative association with agreeableness. In this prison sample, as in non-incarcerated samples, triarchic meanness is closely linked to the FFM construct of antagonism (i.e., low agreeableness; see Poy et al., 2014). Interestingly, and contrary to hypotheses, meanness was uniquely associated with low conscientiousness, even after accounting for its relationship with disinhibition. It may be that the uncaring, detached features of meanness are expressed as disregard for personal responsibilities in the prison context; however, this association did not appear to extend to overt disciplinary problems, given the null correlation between meanness and staff ratings of prison behavior. Finally, meanness was positively associated with all facets of hopelessness but was unrelated to substance problems or self-harm. Meanness includes a prominent element of cynicism that may result in elevated hopelessness scores (e.g., Berg et al., 2013; Sellbom et al., 2018) despite null relations with other distress-related problems.

Consistent with its nomological net, disinhibition was uniquely associated with high neuroticism, low conscientiousness, and low agreeableness. Further, as expected, disinhibition was positively related to substance use problems, hopelessness, and self-harm. This finding is consistent with prior evidence that disinhibition constitutes a liability factor for myriad forms of psychopathology that involve poor emotional or behavioral control (Buchman-Schmitt et al., 2017; Patrick et al., 2013a, b; Perkins et al., 2019). Finally, negative associations were noted for disinhibition with staff ratings of prison behavior and reintegration prognosis. These are consistent with a prior study using structured risk assessments (Sellbom et al., 2018) and may reflect the persistently unrestrained, irresponsible tendencies exhibited by those high in disinhibition both inside and outside the prison setting.

Sex Differences in External Correlates of the Triarchic Traits

Regarding the central theme of the current paper, the main result was that the similarities between sexes outnumbered the differences. First, males and females did not differ in mean scores on TriPM Boldness or Meanness. This finding accords with some prior prison studies utilizing the Psychopathic Personality Inventory (PPI; Lilienfeld & Andrews, 1996), another personality-based measure of psychopathy, which have found few mean-level differences between males and females on fearless dominance (akin to boldness; e.g., Sellbom et al., 2017). However, our result is in contrast to the literature for undergraduates and forensic mental health evaluees reviewed above, in which higher boldness and meanness scores have typically been reported for males as compared to females. One explanation may be that females in our unselected prison sample were less affected by normative gender socialization forces over development than community females, contributing to their engagement in crime as well as their relatively elevated boldness and meanness (see Letendre, 2007; Scott & Mikell, 2019). Relatively similar levels of boldness and meanness across sexes would plausibly be observed in an unselected prison sample such as ours, containing individuals with and without mental illness, but not in a forensic sample (Anestis et al., 2019; Sellbom et al., 2017), in which mental illness may have played a greater role than gender socialization in females’ engagement in crime (Blanchette & Brown, 2019; Fazel & Grann, 2006; Flynn et al., 2011).

As expected, participant sex did not moderate observed relations of boldness with most criterion variables. Boldness is theorized to involve reduced sensitivity of the brain’s defensive reactivity system to cues signaling threat or punishment (e.g., Patrick et al., 2019; Yancey et al., 2016). Operating from this perspective, it appears that dispositional fearlessness manifested similarly for males and females in the current study — except in terms of its impact on staff ratings of behavior within the prison and social connections outside, where in each case associations for boldness were more negative in females than in males. One potential interpretation of this unanticipated result is that some aspects of boldness may be viewed by others as adaptive in males but maladaptive in females; for example, social dominance may be seen by raters as either “leadership” or “pushiness,” depending on the sex of the evaluee. Another possibility is that boldness may be expressed more in terms of manipulativeness or erratic behaviors in incarcerated females than in males. For instance, the affective-interpersonal (Factor 1) features of psychopathy are closely linked to borderline personality disorder symptoms in females, but not males (Verona et al., 2012). Females high in boldness might rely on manipulation or relational aggression to achieve their goals to a greater extent than high-bold males (see also Crick & Grotpeter, 1995; Robbins et al., 2003). These behaviors could plausibly result in poorer social relationships and more disciplinary issues inside the prison. However, since this finding was not hypothesized, it requires replication and should be interpreted with caution until replicated.

Based on the literature, we anticipated that sex would moderate the expression of meanness in particular with regard to distress symptomatology and personality. As meanness involves dysfunction in affective and affiliative systems (Palumbo et al., 2020; Viding & McCrory, 2019), its expression was hypothesized to be influenced by gender norms and females’ socialization to be warm and cooperative (Eagly, 2009). Although no Sex x Meanness interaction effects were significant in this sample, some approached significance, with meanness tending to relate more strongly to increases in BHS Lack of Motivation and decreases in DSHI Versatility in females than males. Although the former effect would be consistent with hypotheses, further research is needed with larger samples to achieve adequate power.

The majority of points of divergence between sexes concerned the trait of disinhibition. First, mean levels of disinhibition were higher for females than males in this prison sample. This finding contrasts with prior research in a forensic mental health sample that demonstrated higher disinhibition among males (Anestis et al., 2019), and with undergraduate samples that showed similar levels across sex (e.g., Drislane & Patrick, 2017). Higher levels of disinhibition may need to be present, on average, for females to engage in crime, given that socialization processes may otherwise inhibit such behavior (Leve et al., 2005).

Sex differences were also observed in the associations of disinhibition with other variables. In particular, TriPM Disinhibition in females was more closely associated with self-harm than in males. Consistent with these findings, impulsivity, aggression, and hostility — constructs central to the nomological network of disinhibition — are more often manifested as self-directed violence and self-harm in females than in males (Sadeh et al., 2011). Related concepts of emotion dysregulation, affective instability, and ineffective emotion regulation strategies are also elevated among females high in psychopathy relative to their male counterparts (de Vogel & Lancel, 2016; Kreis & Cooke, 2011; Sica et al., 2015; Verona et al., 2012). Females may be socialized to express problems through emotional dysregulation (internalizing; Keenan & Shaw, 1997). Another possible explanation involves the fact that disinhibition is influenced by the early environment (Tuvblad et al., 2019) and is correlated with a history of abuse (Gottfried et al., 2019; Graham et al., 2012; Verona et al., 2005). Given that trauma is extremely common among incarcerated females (DeHart et al., 2014; Lynch et al., 2012), such experiences could play a role in the sex-differentiated expression of disinhibition as emotion dysregulation. This explanation could also account for our finding that disinhibition was associated with greater increases in substance use among females than males, as the association between post-traumatic stress and substance use depends on the presence of emotion dysregulation (Tull et al., 2015), especially among women (Bornovalova et al., 2009). Although our substance use results contrast with findings from a forensic mental health clinic sample (Anestis et al., 2019), it is possible that the lower rate of comorbid serious mental illness in our unselected prison sample resulted in clearer sex differences in the degree to which substance use is driven by distress. Nevertheless, as with other mechanistic possibilities offered throughout this paper, these inferences remain to be explicitly tested.

Disinhibition also predicted staff ratings of misbehavior in prison to a greater degree in females than in males. Such a result is particularly important given that among incarcerated females, PCL-R scores do not predict violent behavior, verbal aggression, or noncompliance within the prison setting (Salekin et al., 1997). In this respect, as a trait-based approach rooted in models of personality, the triarchic model may hold promise for improving risk assessment among incarcerated females. However, this result requires replication.

Strengths, Limitations, and Directions

A notable strength of the current study is its use of a mixed-sex prison sample and the examination of external correlates considered to be of particular importance to this population (e.g., substance problems, self-harm, institutional behavior problems). This design allowed us to undertake, for the first time in an unselected prison sample, direct comparisons of the external correlates of the triarchic model across males and females. In addition, our sample was composed of individuals charged with serious crimes and who had several prior convictions; thus, the crime-history profile of our participants was distinctly severe.

The current study also has certain limitations. First, our sample consisted of incarcerated individuals from the nation of Italy, and thus our results may not generalize to individuals from other cultures and ethnic backgrounds. In addition, although the inclusion of staff-rated criterion variables was a strength, the psychometric properties of these measures are unknown, and it is unclear to what degree gender bias may have played a role in ratings. However, the incorporation of multiple sources of data in these ratings (e.g., police reports) may mitigate these concerns somewhat. Finally, although the focus of this study was on external validation, there is also a need for research on the internal psychometric properties of the TriPM in prison samples. This work will require larger samples of incarcerated females in particular (here, n=83) and could include structural analysesFootnote3 and examinations of measurement invariance across sexes. A larger sample would also allow for an examination of the interactive and configural effects of triarchic dimensions (e.g., variants of psychopathy) in predicting important clinical criteria across sex.

Scholars of diversity training, when testing the efficacy of their approaches, too often use proxy measures for success that are far removed from the types of consequential outcomes that reflect the purported goals of such trainings

Diversity Training Goals, Limitations, and Promise: A Review of the Multidisciplinary Literature. Patricia G. Devine and Tory L. Ash. Annual Review of Psychology, Vol. 73:-, publication date January 2022, online on July 19, 2021. https://doi.org/10.1146/annurev-psych-060221-122215

Abstract: In this review, we utilize a narrative approach to synthesize the multidisciplinary literature on diversity training. In examining hundreds of articles on the topic, we discovered that the literature is amorphous and complex and does not allow us to reach decisive conclusions regarding best practices in diversity training. We note that scholars of diversity training, when testing the efficacy of their approaches, too often use proxy measures for success that are far removed from the types of consequential outcomes that reflect the purported goals of such trainings. We suggest that the enthusiasm for, and monetary investment in, diversity training has outpaced the available evidence that such programs are effective in achieving their goals. We recommend that researchers and practitioners work together for future investigations to propel the science of diversity training forward. We conclude with a roadmap for how to create a more rigorous and relevant science of diversity training.

Those who gain a good reputation are often preferred as interaction partners, but excessively generous individuals risk losing their good reputation, and even being vilified, ostracised or antisocially punished

No Good Deed Goes Unpunished: the social costs of prosocial behaviour. Nichola J Raihani & Eleanor A Power- Evolutionary Human Sciences, Jul 2021. DOI: 10.1017/ehs.2021.35

Abstract: Performing costly helpful behaviours can allow individuals to improve their reputation. Those who gain a good reputation are often preferred as interaction partners and are consequently better able to access support through cooperative relationships with others. But investing in prosocial displays can sometimes yield social costs: excessively generous individuals risk losing their good reputation, and even being vilified, ostracised or antisocially punished. As a consequence, people frequently try to downplay their prosocial actions or hide them from others. In this review, we explore when and why investments in prosocial behaviour are likely to yield social costs. We propose two key features of interactions that make it more likely that generous individuals will incur social costs when:  (i) observers infer that helpful behaviour is motivated by strategic or selfish motives; and (ii) observers infer that helpful behaviour is detrimental to them. We describe how the cognition required to consider ulterior motives emerges over development and how these tendencies vary across cultures – and discuss how the potential for helpful actions to result in social costs might place boundaries on prosocial behaviour as well as limiting the contexts in which it might occur. We end by outlining the key avenues and priorities for future research. 

Keywords: prosocial behaviour, reputation, modesty, cooperation, partner choice, morality

Preferences for attractiveness, resources, kindness, intelligence & health in a long-term mate, 45 countries: Each sex tended to report more demanding preferences for attractiveness & resources where the other sex was abundant

Sex differences in human mate preferences vary across sex ratios. Kathryn V. Walter et al. Proceedings of the Royal Society B: Biological Sciences, Jul 21 2021. https://royalsocietypublishing.org/doi/10.1098/rspb.2021.1115

Abstract: A wide range of literature connects sex ratio and mating behaviours in non-human animals. However, research examining sex ratio and human mating is limited in scope. Prior work has examined the relationship between sex ratio and desire for short-term, uncommitted mating as well as outcomes such as marriage and divorce rates. Less empirical attention has been directed towards the relationship between sex ratio and mate preferences, despite the importance of mate preferences in the human mating literature. To address this gap, we examined sex ratio's relationship to the variation in preferences for attractiveness, resources, kindness, intelligence and health in a long-term mate across 45 countries (n = 14 487). We predicted that mate preferences would vary according to relative power of choice on the mating market, with increased power derived from having relatively few competitors and numerous potential mates. We found that each sex tended to report more demanding preferences for attractiveness and resources where the opposite sex was abundant, compared to where the opposite sex was scarce. This pattern dovetails with those found for mating strategies in humans and mate preferences across species, highlighting the importance of sex ratio for understanding variation in human mate preferences.

4. Discussion

The consequences of sex ratio skew have long been of interest to scientists of evolution and behaviour, and particularly of interest to those who study mating [18,58]. Additionally, more recent work has examined the complex role of mate scarcity or abundance in patterns of sex differentiated reproductive behaviour, such as mate competition and parental care across species [59]. Despite these important advances, empirical work connecting human mate preferences to sex ratio remains scarce (for review, see [60]). Here, we attempted to address this literature gap with a large, cross-cultural investigation of human mate preferences. Overall, we found that sex differences in mate preferences vary across sex ratios. Where men are numerous, compared to where they are scarce, men tended to have lower absolute preferences for physical attractiveness, whereas women tended to have higher preferences. This inverse relationship also held for relative preferences for both physical attractiveness and good financial prospects. In sum, each sex tended to report more demanding preferences for attractiveness and resources where they had more power of choice on the mating market, compared to where they had less mating market power.

These findings are important for several reasons. First, the pattern whereby the scarcer sex sets more demanding preferences falls parsimoniously in line with patterns found for mating strategies in humans [15,17], and for mating systems, mate competition and mate preferences in non-humans [3,5,6]. While this study is correlational in nature and cannot speak to causality, the pattern of results is what would be expected if preferences for attractiveness and resources were calibrated to mate availability, and thus plastic in response to mating market demand.

Second, as we show that men's and women's preferences vary across sex ratios inversely, the magnitude of average sex differences in preferences also varies. Much research has examined the universality of sex differences in human mate preferences [21,61]. Less research has examined the variation in sex differences across cultures. The fact that sex ratio has the power to predict cross-cultural variation in mate preferences attains special importance as two previously reported sources of variation, pathogen prevalence and gender equality, have recently failed to replicate as predictors of cross-cultural variation in human mate preferences [22,44,62,63].

Third, that sex ratio more clearly predicts variation in relative preferences than in absolute preferences has implications for the measurement and analysis of mate preference variables. While absolute preferences reflect the trait values that people desire in potential mates, they do not as directly indicate how demanding that preference is within a particular environment. For instance, a strong preference for kindness (7 on a 7-point scale) may correspond to an extremely demanding preference in an environment where the average kindness is 4 on the same scale, or a somewhat demanding preference if the average kindness is 6 on the same scale. Given that scarcity on the mating market is hypothesized to afford power to express more stringent demands, measuring preferences in absolute terms might miss out on a critical dimension of variation relevant to sex ratio. Relative preferences, which incorporate information about the distribution of local trait values, may provide a more relevant measure of preferences because they more directly measure how demanding a given preference value is in a participant's local context.

Despite these important findings, the study does have some limitations and leaves open some important questions. First, the relationship between sex ratio and mate preferences was not as robust for some mate preference dimensions: kindness, health and intelligence. One possibility for why the same pattern did not emerge for these preferences is because they are so highly desired, and therefore more invariant. Indeed, the mean preference for kindness across all countries was, on a 7-point scale, M = 6.23, 95% CI [6.21, 6.26], Mdn = 6, for women, and M = 6.12, 95% CI [6.10, 6.15], Mdn = 6, for men. These universal near-ceiling effects leave limited room for variation. Furthermore, kindness, health and intelligence are also qualities considered very important for both men and women, and therefore these preferences may be less likely to shift downward, even when market power is low [21,64]. Future research could examine the relationship between sex ratio and a wider range of mate preferences—crucially, including those that exhibit more variation—to determine the extent of the relationship between mate preferences and sex ratio.

Second, our finding that mate preferences vary according to current sex ratio at birth could be considered somewhat surprising. Theoretically, sex ratio at birth, the number of males born for every 100 females born, does not appear to typify the conceptual variable of interest: the number of mates available to members of each sex. However, sex ratio at birth is moderately correlated with the other measures of sex ratio (r = 0.35, adult sex ratio; r = 0.39, sex ratio 15–49; r = 0.38, sex ratio 15–65; r = 0.16, city sex ratio), so it may be capturing sex ratio variation similar to adult sex ratio measures. Additionally, sex ratio at birth is an important variable to consider because it may be the origin of some skewed adult sex ratios, particularly in countries with an abundance of men. In particular, sex ratio at birth may reflect aspects of gender relations. Though skewed sex ratios can occur because of migration, violence and unbalanced death rates, sex ratio can also vary due to cultural practices such as sex selective abortions based on preferences for sons [65]. Some prior work has hypothesized that in places where women are scarce, women may have less structural power overall, and may be unable to fulfil their mate preferences even when they hold mating market power [18]. Although we did not find evidence consistent with this hypothesis—women's preferences tended to increase (not decrease) as they became scarcer—future work should continue to explore the source of sex ratio at birth's predictive power, including its potential relationship to gender equality.

Relatedly, our data do not speak to how the relationship between sex ratio and mate preferences emerges. One possibility is that the effects of sex ratio reflect evoked culture, and mating psychology reacts facultatively to local sex ratio to calibrate mate preferences. Alternatively, this relationship could reflect transmitted culture if, for example, people with less strict preferences tend to experience greater mating success when their own sex is abundant, and others mimic their preferences via prestige-based learning [66]. These possibilities are each equally consistent with the data we have here. Future research should explore further the particular ontogenetic mechanisms responsible for cross-cultural variation in preferences.

Furthermore, sex ratio measurement is made complicated by the fact that previous research has varied in the way sex ratio is defined. In particular, prior studies vary with respect to the age ranges used to estimate sex ratio, and whether operational sex ratio (only individuals able to reproduce) or adult sex ratio (all individuals considered adults, including elderly), is the key measure of sex ratio. Some of the inconsistent results in the prior literature may be due to researchers' use of only a single measure of sex ratio, which at times may fail to accurately capture the conceptual variable of interest: the availability of potential mates. Here we attempted to address this limitation by operationalizing country-level sex ratio measures in a variety of ways, and including city-level sex ratio and sex ratio at birth. By taking a broad approach to measuring sex ratio, we showed that results tended to remain robust across measures, though there were exceptions. However, a limitation of this broad approach is that it remains unclear what precisely is the best way to measure sex ratio for human mating research—a question future research must explore.

Part of the lack of clarity about how to operationalize sex ratio comes from the lack of clarity about how humans actually track mate availability. Country-level measures, or even city-level measures of sex ratio, may not accurately represent the sex ratios experienced and tracked by individual participants. More precise sex ratio measurements may produce different results than those found here.

Overall, the consequences of sex ratio have been well studied across mating behaviour in the non-human literature, from intrasexual competition, to preferences, to mating system [3,5,6]. The consequences of sex ratio have also been examined in the human literature in areas spanning from violence to financial behaviour or mating strategy [15,67,68]. However, the question of how sex ratio relates to human mate preferences has received limited attention and prior findings have lacked clarity. Here we provided evidence that sex ratio is related to mate preferences across cultures, such that where each sex is scarce, that sex tends to have higher preference demands for attractiveness and resources. These findings further elucidate the nature of human mating psychology, in particular its universal structure and systematic variation.

Due to the social desirability bias, software pirates deny it when filling surveys; 47pct actual piracy rate vs 19pct self-reported piracy rate

Liar, liar, pants on fire! Social desirability bias in software piracy research. Marton Gergely & V. Srinivasan (Chino) Rao. Behaviour & Information Technology, Jul 19 2021. https://doi.org/10.1080/0144929X.2021.1950834

Abstract: Measures of ethical behaviours in research may be subject to social desirability bias (SDB). Most behavioural aspects of software piracy research are a subset of ethical research. Few studies of software piracy have explicitly addressed the issue of SDB. In this article, the extent of SDB that may be present in software piracy is empirically assessed. This was done by comparing SDB in software piracy under three conditions using the 40-item Balanced Inventory of Desirable Responding (BIDR) scale. First, software piracy behaviour was examined in an experimental setting with actual money at stake. This allowed subject behaviour to be observed rather than inferred from self-report responses. Second, a survey was conducted to test the extent of software piracy based on subject self-report responses. Third, the extent of software piracy was also assessed based on peer-report responses (i.e.: the subject reported whether their peers would pirate). A comparison of the responses in the three conditions allows us to draw inferences about SDB in software piracy research. Self-report surveys exhibited high levels of SDB. The behaviour in the experimental condition, and responses in the peer-report survey method, did not exhibit SDB.

Keywords: Software piracyinformation system ethicsdigital mediaintellectual property theftsocial desirability bias

Haptic stimulation of endorphin acts to bond relationships in primates and humans; humans have found ways to trigger the endorphin system virtually without touch, allowing us to ‘groom’ at a distance with more individuals

Virtual touch and the human social world. Robin IM Dunbar. Current Opinion in Behavioral Sciences, Volume 43, February 2022, Pages 14-19. https://doi.org/10.1016/j.cobeha.2021.06.009

Highlights

• Haptic stimulation of endorphin acts to bond relationships in primates and humans.

• Humans have found ways to trigger the endorphin system virtually without touch.

• Virtual ‘touch’ allows humans to ‘groom’ at a distance with more individuals.

Abstract: Touch forms a central component of social bonding, both in primates and in humans, via the brain’s endorphin system. In primates, this involves social grooming, acting via the CT neuron system. Although humans still use soft touch for bonding relationships, they have had to find ways of triggering the endorphin system without the need for physical touch in order to be able to increase the size of their social groups beyond the size of those characteristic of monkeys and apes. These behaviors include laughter, singing, dancing, the rituals of religion, feasting and emotional storytelling, and act functionally as a form of ‘virtual touch’. I summarise recent behavioral, neurobiological and genetic evidence demonstrating that these behaviors both enhance bonding and act through the endorphin system.

Reviewing theory and experimental evidence, they suggest that spontaneous BOLD activity may be more closely aligned with off-line plasticity and homeostatic processes than on-line fluctuations in cognitive content

Brain activity is not only for thinking. Timothy OLaumann, Abraham ZSnyder. Current Opinion in Behavioral Sciences, Volume 40, August 2021, Pages 130-136. https://doi.org/10.1016/j.cobeha.2021.04.002

Abstract: The human brain is a complex organ with multiple competing imperatives. It must perceive and interpret the world, incorporate new information, and maintain its functional integrity over the lifespan. Neural activity is associated with all of these processes. Spontaneous BOLD signals have been invoked as representing neural activity associated with all of these processes. However, their exact role in these processes remains controversial. Here, we review learning machine theory, molecular mechanisms of synaptic plasticity and homeostasis, and recent experimental evidence to suggest that spontaneous BOLD activity may be more closely aligned with off-line plasticity and homeostatic processes than on-line fluctuations in cognitive content.

Introduction

The existence of unceasing spontaneous brain activity has been recognized since at least the 1930s [1]. However, the functions of this activity have remained mysterious [2]. Over the last three decades, blood oxygen level dependent (BOLD) fMRI has become the dominant tool for measurement of brain activity in humans. Soon after the adoption of fMRI, it was observed that fMRI signals exhibit constant fluctuations unrelated to the task [3]. In the context of task fMRI, this activity was conventionally regarded as ‘physiological noise’ [4]. However, it is now clear that this ‘physiological noise’ is temporally correlated within functional systems [5,6]. It is this property of spontaneous brain activity that constitutes the basis of resting state functional connectivity (RSFC) [7]. The existence of this well-structured organization implies that spontaneous brain activity is physiologically consequential.

The meaning of spontaneous BOLD signal fluctuations has been variably interpreted along two different perspectives. According to one view, spontaneous BOLD fluctuations are proposed to reflect unconstrained cognitive processes, for example, retrospection, prospection, reflection, environmental monitoring — the ‘stream of consciousness’ — attendant to our subjective experience. Given the centrality of perception and action to mental life, it is appealing to assume that all observed brain activity is directly related to moment-to-moment cognition and behavior. This perspective has been reinforced by a massive accumulation of PET and fMRI experiments in which brain activity has been imaged with the objective of localizing cognitive operations [8]. More recently, the observation of ‘dynamic’ functional connectivity during wakeful rest and changes in functional connectivity between rest and task states have, at times, been interpreted as reflecting cognition [9,10].

We have previously articulated several problems with the notion that all ongoing BOLD activity directly reflects cognition and behavior (Box 1; [11]): (1) The topography of BOLD fMRI correlations remains largely intact during slow-wave sleep [12] and even anesthesia [13], states in which cognition is presumed to be either absent or greatly attenuated; (2) The extent to which task paradigms modify the correlation structure of spontaneous BOLD signal fluctuations is very limited [14,15,16•]; (3) While unconstrained cognition might be expected to vary from scan to scan within an individual, RSFC remains remarkably consistent across sessions [17,18]. RSFC is also relatively stable within a given scan, discounting fluctuations attributable to drowsiness [11] or arousal [19], which likely relate to fluctuations in BOLD signals, at least partly due to alterations in respiratory behavior and pCO2 [20]. Moreover, brain metabolic activity is high at all times and minimally affected by task performance [21].

Box 1

Evidence that RSFC structure is largely independent of cognitive content

1.

RSFC structure is similar during wake and sleep. For instance, DMN structure is observed through wake, S1, S2, and SWS [12,100].

2.

RSFC structure is present under anesthesia [13,101], although covariance does diminish with increased sedation [102].

3.

RSFC structure is minimally altered by task state [14, 15].

4.

RSFC structure within subject is consistent across sessions [16,11,103].

5.

RSFC structure within subject is similar over long time scales [18,17].

6.

RSFC structure is consistent across subjects at the population level [104,105].

7.

Similar RSFC structure is evident across mammalian species [106, 107, 108].

For all of these reasons, unconstrained cognition does not fully explain ongoing spontaneous activity. An alternative view proposes that spontaneous BOLD activity may more closely relate to mechanisms associated with learning and memory [22•,23]. In the following, we review prior literature supporting the perspective that a substantial fraction of spontaneous brain activity represents homeostatic and consolidative signaling, the function of which is to enable neural plasticity while maintaining the brain's functional integrity through time. We also review recent evidence that BOLD RSFC may be intimately tied to these processes.

Learning machine theory

When considering the role of ongoing neural activity in brain function, it is important to recognize that one of the brain’s primary capacities is its ability to learn new information about its environment. Theoretical considerations, initially formulated by David Marr [24], suggest that any associative learning machine functions optimally if it is allowed to alternate between two states: (1) a learning phase, during which the machine is connected to inputs and connections are enhanced between simultaneously active elements and (2) a restorative phase during which the machine is disconnected from inputs and connections between elements are rebalanced in a manner that increases randomness (entropy) [25,26•]. In multi-layer perceptrons, this principle is expressed as iterative alternation between a forward phase, during which prediction error is evaluated, and a backward phase, during which connection weights are adjusted by back-propagation [27]. The starkest expression of the state alternation principle in living organisms is sleep versus wake. This alternation appears to be necessary: all organisms capable of learning alternate between wake versus sleep states [28]. In vertebrates, events experienced during wake are registered in the hippocampus and the cerebral cortex [29,30]. During slow wave sleep (SWS), reactivation of the same circuits leads to the creation of stable (consolidated) episodic memory [31•].

Understanding how state alternation is implemented in brains requires consideration of the cellular and molecular events underlying synaptic weight modification. Activity-dependent synaptic plasticity plays a crucial role in brain development well before birth [32, 33, 34]. For example, retino-tectal connections have been shown to be sculpted by spontaneous retinal waves during prenatal development of the visual system [35]. Following birth, spontaneous activity continues to refine neural connections using sensory feedback [36,37]. During early life critical periods, experience-dependent synaptic plasticity tunes the response properties of cortical sensory neurons (e.g. ocular dominance columns) [38]. As the brain matures, metabolic ‘brakes’ limit neural plasticity to mechanisms centered on inhibitory interneurons [39, 40, 41]. Although neural plasticity in adults is more restricted, the underlying activity-dependent processes likely follow similar principles.

Molecular mechanisms of activity-dependent synaptic plasticity

Activity-dependent synaptic plasticity is conventionally discussed under the headings of long-term potentiation (LTP) and long-term depression (LTD). But LTP/LTD are deceptively simple terms encompassing a wide range of molecular processes [42,43]. The early phase of LTP (E-LTP) is triggered by Ca2+ influx linked to post-synaptic depolarization, which sets in motion molecular cascades mediated by phosphorylation and dephosphorylation of regulatory molecules (e.g. protein kinase C (PKC) and Ca2+-calmodulin-dependent protein kinase (CamKII)) that govern neurotransmitter receptor trafficking. E-LTP lasts 1−3 hours and is independent of gene expression. The late phase of LTP (L-LTP) begins with the transcription of immediate early genes (IEGs; e.g. Arc, Zif268) that control translational processes, which lead, on a time scale of hours, to structural changes in dendritic spines [44, 45, 46]. Thus, whereas electrophysiological event-related responses may last up to a few hundred millisec and BOLD hemodynamic responses typically evolve over ∼16−20 s, the metabolic traces of the evoked activity persist over much longer time scales. These traces may underlie the observation that fMRI responses to task A are modulated by having performed unrelated task B during the past half hour [47].

The Hebbian principle (‘fire together → wire together’) is often invoked to account for resting state functional connectivity [48,49]. The mechanism underlying Hebbian learning, that is, spike-timing dependent synaptic plasticity (STDP), has been elucidated in considerable detail [50,51]. In brief, neural back-propagation of depolarization induced by a first excitatory stimulus removes the Mg2+ block at NMDA receptors, thereby allowing a second stimulus (if it occurs within a 20–85 ms window) to induce local Ca2+ entry, which initiates the LTP molecular cascade, ultimately reinforcing the association between the paired stimuli. Hebbian mechanisms undoubtedly play a central role in adult learning. Accordingly, it is reasonable to posit that synchronous spontaneous BOLD fluctuations that give rise to RSFC are due to a history of prior co-activation. However, a system dominated by unopposed Hebbian plasticity inevitably becomes either infinitely active or silent.

In contrast to Hebbian plasticity, which adjusts synaptic weights in the same direction as an applied stimulus, the brain also employs various mechanisms of homeostatic plasticity, which adjusts synaptic strengths in the opposite direction to return excitatory/inhibitory (E/I) balance and mean firing rate to prior set points [52]. Homeostatic plasticity includes cell-autonomous mechanisms that directly adjust neuronal excitability to counteract environmental stimuli, as well as multiplicative synaptic scaling, which preserves relative strengths between neighboring synapses, thereby maintaining currently represented information [53•]. These homeostatic mechanisms operate at the level of dendritic branches [45], individual neurons [53•], and large-scale circuits [54], and are active over multiple time scales [55,56]. A correlate of these homeostatic processes is ongoing turnover of synaptic proteins and lipids with half-lives on the order of ‘minutes, hours, days, weeks’ [57]. Modeling experiments suggest that homeostatic regulation of E/I balance plays a crucial role in maintaining the characteristic features of spontaneous brain activity [58]. Importantly, synaptic homeostasis is inseparable from consolidation, the process whereby brief changes in neural activity ultimately lead to stable memory [59,60•]. Thus, it is reasonable to posit that spontaneous activity includes both Hebbian and homeostatic signaling.