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.
Highlights
It is unknown how the brain coordinates decisions to withstand personal costs in order to prevent other individuals’ distress
We examined nine brain areas chosen for their known involvement in self-reported human empathy/ social behavior or negative emotion in humans and rodents: anterior cingulate (ACC), anterior insula (INS), orbitofrontal cortex (OFC), infralimbic cortex (INF), prelimbic cortex (PRE), paraventricular nucleus of the hypothalamus (PVN), olfactory amygdala (OAMY), central nucleus of the amygdala (CE), and basolateral nucleus of the amygdala (BLA) (Kim et al, 2015; Rilling & Sanfey, 2011; Stowers, Cameron, & Keller, 2013)
Our elastic net (ENET) procedure modeled the relationship between Intersubjective Avoidance” (IA) (7 rats across 10 Testing days, for a total of 70 behavioral data points) and (1) the power in 1 Hz-wide oscillation bands from 1 to 100 Hz averaged across all the electrodes implanted in each of the ACC, OFC, INS, BLA, and OAMY (1000 predictors when all electrodes in a brain region are averaged) and (2) the magnitude of coherence in 1 Hz oscillation bands from 1 to 100 Hz in each possible pair of these brain regions (4500 predictors when all electrodes in a brain region are averaged) (Figure 4e)
Summary
“Empathy” is an innate, fundamental phenomenon that confers powerful evolutionary advantage. It is difficult to test relationships between coherence and intersubjective decision-making in rodents, due to the challenges in developing appropriate behavioral, recording, and analysis techniques for assessing LFP activity in multiple brain regions simultaneously while rodents make intersubjective decisions. Intersubjective decision-encoding oscillations were observed primarily when rats were witnessing another rat get shocked, rather than when rats had already chosen to avoid another rat’s pain, supporting the inference that the oscillations were related to the integration of social cues with neural decision-making machinery, rather than some type of generalized arousal These results suggest that the brain networks involved in rat intersubjective decision-m aking may be evolutionarily conserved, and provide evidence that intersubjective decisions are encoded through interactions between brain regions as well as through isolated neural activity
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