Rat intersubjective decisions are encoded by frequency‐specific oscillatory contexts

Abstract

IntroductionIt is unknown how the brain coordinates decisions to withstand personal costs in order to prevent other individuals’ distress. Here we test whether local field potential (LFP) oscillations between brain regions create “neural contexts” that select specific brain functions and encode the outcomes of these types of intersubjective decisions.MethodsRats participated in an “Intersubjective Avoidance Test” (IAT) that tested rats’ willingness to enter an innately aversive chamber to prevent another rat from getting shocked. c‐Fos immunoreactivity was used to screen for brain regions involved in IAT performance. Multi‐site local field potential (LFP) recordings were collected simultaneously and bilaterally from five brain regions implicated in the c‐Fos studies while rats made decisions in the IAT. Local field potential recordings were analyzed using an elastic net penalized regression framework.ResultsRats voluntarily entered an innately aversive chamber to prevent another rat from getting shocked, and c‐Fos immunoreactivity in brain regions known to be involved in human empathy—including the anterior cingulate, insula, orbital frontal cortex, and amygdala—correlated with the magnitude of “intersubjective avoidance” each rat displayed. Local field potential recordings revealed that optimal accounts of rats’ performance in the task require specific frequencies of LFP oscillations between brain regions in addition to specific frequencies of LFP oscillations within brain regions. Alpha and low gamma coherence between spatially distributed brain regions predicts more intersubjective avoidance, while theta and high gamma coherence between a separate subset of brain regions predicts less intersubjective avoidance. Phase relationship analyses indicated that choice‐relevant coherence in the alpha range reflects information passed from the amygdala to cortical structures, while coherence in the theta range reflects information passed in the reverse direction.ConclusionThese results indicate that the frequency‐specific “neural context” surrounding brain regions involved in social cognition encodes outcomes of decisions that affect others, above and beyond signals from any set of brain regions in isolation.

Beyond Emotions: Oscillations of the Amygdala and Their Implications for Electrical Neuromodulation

“…Avoidance of shock delivery to a fellow rat was linked to low gamma coherence between the insula, OFC and BLA, whereas choices, which resulted in another rat receiving a shock, were linked to increased gamma coherence between the same regions. Interestingly, high gamma oscillations in the BLA preceded those in the insula (Schaich Borg et al, 2017). In addition, stronger alpha power was observed in several brain regions, including the amygdala, and correlated positively with avoidance of shock delivery.…”

“…In addition, stronger alpha power was observed in several brain regions, including the amygdala, and correlated positively with avoidance of shock delivery. Within the network of interest, the amygdala seemed to be the source of alpha oscillations as its activity preceded alpha oscillations measured in other brain areas (Schaich Borg et al, 2017). Theta oscillations that have been observed in rats in a social fearful context (Tendler and Wagner, 2015) were measured in the BLA and correlated negatively with the shock avoidance behavior described above (Schaich Borg et al, 2017).…”

“…Furthermore decreases in alpha frequencies have been linked to PD-associated dementia (Cozac et al, 2016). In a rat study, the BLA has been the source of alpha oscillations during social decisions, entraining connected regions (Schaich Borg et al, 2017). Alpha frequency entrainment of motor regions by the amygdala would be an interesting mechanism to improve cognitive functions in PD patients suffering from dementia.…”

Rat behavior and dopamine release are modulated by conspecific distress

“…However, it is unclear how neurobiological substrates integrate harm of others into our decisions because detailed work in animals at the single-unit and neurotransmitter level has not yet occurred. A growing number of high-profile reports have demonstrated that rodent models can be used to perform such experiments ( Atsak et al, 2011 ; Ben-Ami Bartal et al, 2011 ; Ben-Ami Bartal et al, 2014 ; Burkett et al, 2016 ; Church, 1959 ; Guzmán et al, 2009 ; Hernandez-Lallement et al, 2018 ; Hernandez-Lallement et al, 2018 ; Hernandez-Lallement et al, 2017 ; Jeon et al, 2010 ; Jones et al, 2014 ; Kashtelyan et al, 2014 ; Kim et al, 2010 ; Langford et al, 2006 ; Masserman et al, 1964 ; Meyza et al, 2017 ; Mogil, 2015 ; Panksepp, 2011 ; Panksepp and Lahvis, 2011 ; Sato et al, 2015 ; Schaich Borg et al, 2017 ). For example, rats have been described as ‘empathetic’ and ‘prosocial’ because they freeze when they see others freeze in response to threat and will rescue conspecifics from distress when given the opportunity ( Atsak et al, 2011 ; Ben-Ami Bartal et al, 2011 ; Ben-Ami Bartal et al, 2014 ; Meyza et al, 2017 ).…”

Bidirectional and context-dependent changes in theta and gamma oscillatory brain activity in noradrenergic cell-specificHypocretin/Orexin receptor 1-KO mice

“…Furthermore, increasing evidence suggests that oscillatory patterns are active functional determinants of brain circuits processing, and their behavioral outcomes, e.g. [3][4][5][6] .…”