Voluntary Enhancement of Neural Signatures of Affiliative Emotion Using fMRI Neurofeedback

Abstract

In Ridley Scott’s film “Blade Runner”, empathy-detection devices are employed to measure affiliative emotions. Despite recent neurocomputational advances, it is unknown whether brain signatures of affiliative emotions, such as tenderness/affection, can be decoded and voluntarily modulated. Here, we employed multivariate voxel pattern analysis and real-time fMRI to address this question. We found that participants were able to use visual feedback based on decoded fMRI patterns as a neurofeedback signal to increase brain activation characteristic of tenderness/affection relative to pride, an equally complex control emotion. Such improvement was not observed in a control group performing the same fMRI task without neurofeedback. Furthermore, the neurofeedback-driven enhancement of tenderness/affection-related distributed patterns was associated with local fMRI responses in the septohypothalamic area and frontopolar cortex, regions previously implicated in affiliative emotion. This demonstrates that humans can voluntarily enhance brain signatures of tenderness/affection, unlocking new possibilities for promoting prosocial emotions and countering antisocial behavior.

Empathic Care and Distress: Predictive Brain Markers and Dissociable Brain Systems

“…During presentation of the biographies, empathic care tended to steadily increase, negative emotions tended to rise and fall, and positive emotions tended to rise towards the end of biographies (Figure 5a and Figure S3). Overall, our findings agrees with previous work showing that compassion and affiliative emotion do not have a clear, consistent valence (Condon & Barrett, 2013; Moll et al, 2012, 2014). …”

“…To identify regions selective for empathic care, we identified those that (a) had significantly more positive weights for the empathic care marker than for the distress marker in the multivariate patterns, and (b) were significantly positively correlated with empathic care in univariate voxel-by-voxel analyses, both when controlling and not controlling for distress (see Experimental Procedures). This conjunction revealed that empathic care was preferentially related to activity in mOFC, vmPFC, VS, and septal area (Figure 3a, Figure 4, Table S2), consistent with prior associations of these regions with positive empathic affect, prosocial behavior, and affiliative emotion and behavior (Bredewold et al, 2015; Genevsky & Knutson, 2015; Genevsky et al, 2013; Harbaugh et al, 2007; Hare et al, 2010; Inagaki & Eisenberger, 2012; Klimecki, Leiberg, Lamm, & Singer, 2012; Klimecki, Leiberg, Ricard, & Singer, 2014; Krueger et al, 2007; Moll et al, 2012, 2014, 2006; Morelli et al, 2015; Numan, 1988; Zaki & Mitchell, 2011). Empathic care also was associated with precuneus/posterior cingulate activity, a key node of the mentalizing system often active in response to observing emotional suffering (Bruneau, Dufour, & Saxe, 2013; Bruneau, Dufour, et al, 2012; Bruneau, Pluta, et al, 2012; Immordino-Yang et al, 2009; Masten et al, 2011; Meyer et al, 2013; Morelli et al, 2014).…”

“…This can enable a cumulative science that ultimately produces rigorously validated markers ready for translational use. In the domain of empathy, validated predictive markers may aid in the diagnosis or prognosis of empathy-related disorders (i.e., autism or psychopathy), serve as proximal biological targets for interventions seeking to enhance compassion (Ashar, Andrews-Hanna, Yarkoni, et al, 2016; Klimecki et al, 2012, 2014; Lutz et al, 2008; Weng et al, 2013), or as targets for biofeedback-based training programs aiming to enhance empathy (Moll et al, 2014; Yao et al, 2016). The markers presented here are a first step in a cumulative process of refinement and validation.…”

“…Converging evidence suggests that this region plays a unique role in affiliative behavior across species. In humans, multiple fMRI investigations have linked this area with trust (Krueger et al, 2007), charitable donation (Moll et al, 2006), prosocial behavior (Morelli et al, 2014), giving support to a romantic partner (Inagaki & Eisenberger, 2012), and affiliative emotion (Moll et al, 2012, 2014). In rats, lesioning and pharmacological manipulations of the septal area suggest a causal relationship with the expression of various affiliative and social behaviors, especially maternal behaviors (Sheehan & Numan, 2000).…”

“…Neuroimaging investigations of altruistic and prosocial behavior, which may be preferentially linked to care rather than to distress, have linked these behaviors to the mesolimbic dopamine system, including the ventral tegmental area (VTA), ventral striatum (VS), and ventromedial prefrontal cortex (vmPFC) (Harbaugh, Mayr, & Burghart, 2007; Hare, Camerer, Knoepfle, & Rangel, 2010; Moll et al, 2006; Morelli, Sacchet, & Zaki, 2015; Zaki & Mitchell, 2011), especially in the context of positive affect (Genevsky & Knutson, 2015; Genevsky, Västfjäll, Slovic, & Knutson, 2013). In addition, a septal/anterior hypothalamic circuit has been linked to a range of affiliative emotions and behaviors across species, including maternal and juvenile play behavior in rats (Bredewold, Schiavo, van der Hart, Verreij, & Veenema, 2015; Numan, 1988), and in humans, trust (Krueger et al, 2007), charitable donation (Moll et al, 2006), prosocial behavior (Morelli, Rameson, & Lieberman, 2014), support giving (Inagaki & Eisenberger, 2012), and affiliative emotion (Moll et al, 2012, 2014). …”