Empathy is induced by synchronized neural oscillations in the right hemisphere of the brain


A research team led by Dr. SHIN Hee-Sup at the Center for Cognition and Sociality (CCS) within the Institute for Basic Science (IBS) in Daejeon, South Korea has discovered the underlying neural mechanism that allows us to feel empathy.

The group’s study on mice hinted that empathy is induced by the synchronized neural oscillations in the right hemisphere of the brain, which allows the animals to perceive and share each other’s fear.

Empathy is the ability that allows us to perceive and understand another individual’s emotions, such as joy, sadness, or fear. It is an essential function for human sociality, and its impairment has been observed in numerous psychiatric and neurological disorders such as autism, schizophrenia, and Alzheimer’s disease.

The precise mechanisms within the brain that form the basis of empathy have not been identified, and few studies have been conducted on uncovering its origins.

This capacity to sense the feelings of others is not unique to humans, and its biological mechanisms are shared with other mammals including rodents. ‘Observational fear’, which is a rodent model for emotional contagion, is the basic form of affective empathy. This model has been well-established and is frequently used for studying the neurobiology of empathy.

During the observational fear experiment, a “demonstrator” mouse is given an electric shock, while an “observer” mouse watches from behind a transparent screen. When witnessing another animal receiving a shock, the observer mouse displays an immediate fear response, as demonstrated by its freezing behavior. The observer mouse is also known to be able to recall the experience at a later time.

The CCS-IBS team led by Dr. SHIN Hee-Sup combined this observational fear model with optogenetic experiments to explore the origin of empathy. Notably, this study showed that the synchronized brain rhythms within multiple brain areas are essential for triggering empathy.

In particular, the synchronization between the anterior cingulate cortex (ACC) and basolateral amygdala (BLA) is unique to empathic fear by indirect exposure to others’ distress, not to fear by first-hand experience.

First, they showed that the reciprocal circuit between the ACC-BLA in the right hemisphere is essential for observational freezing behavior. When they optogenetically inhibited the ACC-BLA circuits only in the right brain, mice showed reduced observational freezing. On the other hand, the mice were unaffected when only the left side was inhibited.

Furthermore, the researchers recorded electroencephalogram (EEG) in the ACC and BLA. As a result, they found that brain rhythms with the range of 5-7 Hz selectively increased in the ACC and BLA at the specific moment within the observer mice at the time they showed empathic freezing behavior.

On the other hand, the demonstrator mice which experienced the electric shock first hand showed increase in the lower 3-5 Hz range only within the BLA but not in the ACC.

Dr. Shin, states, “Synchronous neural oscillations within the networks could allow enhanced communications among multiple brain areas for various cognitive and emotional functions. However, their causal relationship has rarely been demonstrated.”

To test the causal relationship between 5-7 Hz rhythms and empathic behavior, the team performed an experiment called ‘closed-loop manipulations’, which involves using optogenetics to inhibit specific neural functions and monitoring the brain waves using EEG (Figure 2B).

Through the closed-loop experiment, they could selectively disrupt 5-7 Hz rhythms in the ACC-BLA circuit, which in turn resulted in significant impairment of observational fear induced freezing during the conditioning sessions. These results indicate that 5-7 Hz rhythms in the ACC-BLA circuit are causally involved in empathic behaviors.

As such, the researchers hypothesized that hippocampal theta (4-12 Hz) rhythms may tune the synchronized activities within the ACC-BLA circuit. It has been suggested that hippocampal theta rhythm provides an oscillatory framework that synchronizes activities between different brain areas.

They selectively modulated the lower range of hippocampal theta by optogenetic manipulations during observational fear. Following the changes in hippocampal theta power, 5-7 Hz rhythm in the ACC-BLA circuits and empathic responses were bi-directionally modulated.

This study strongly indicates that hippocampal-dependent 5-7 Hz synchronized oscillations in the ACC-BLA specifically drive empathic responses in mice.

Dr. Hee-Sup Shin remarked, “Considering the universality of observational fear across mammals, it is reasonable to suppose a similar neural signature critical for affective empathy may be found in humans and could be used to identify empathy dysfunction in humans with psychiatric disorders involving severe social deficits.”

He added, “At the moment, we do not know how hippocampal theta rhythms control the ACC-BLA rhythms. Future studies should address how multiple brain regions are simultaneously mobilized during observational fear.”

Feeling other individuals’ pain and suffering, known as pain empathy, facilitates human social interactions. Empathy has received great attention in the past two decades and neuroscientific studies have demonstrated the involvement of several different underlying brain networks suggesting two subsystems for empathy:

(a) an emotional component involving sensory and affective neural substrates such as the sensorimotor cortex, anterior insula, and anterior and middle cingulate cortex (ACC and MCC); and

(b) a higher-order cognitive component that reflects vicarious understanding and theory of mind (TOM) involving regions such as the precuneus/posterior cingulate cortex, temporoparietal junction, and prefrontal cortex (Jackson et al., 2005; Cheng et al., 2008; Shamay-Tsoory et al., 2009; Lamm et al., 2011; Bernhardt and Singer, 2021; Zhou and Han, 2021).

Furthermore, a number of these brain regions were examined by transcranial magnetic stimulation revealing their causal role in pain empathy and empathic behavior (Avenanti et al., 2005; Gallo et al., 2018; Yang et al., 2018; Zeugin et al., 2020). So far, electroencephalography (EEG) and magnetoencephalography (MEG) studies on empathy for vicarious pain mainly reported modulation of central-parietal-sensory alpha frequency band (7–13 Hz) oscillations (mu rhythm) suggesting that this phenomenon reflects embodied simulation, in line with the prominent affective (i.e., embodied simulation)-cognitive (i.e., mentalizing) empathy model (Perry et al., 2010; Whitmarsh et al., 2011; Woodruff et al., 2011; Chen et al., 2012; Hoenen et al., 2015; Motoyama et al., 2017; Rieèanskı and Lamm, 2019).

The rationale behind the phenomenon of pain empathy mainly relies on the resonance/mirroring phenomenon during which the observation of vicarious pain elicits painful sensations in the observer (Osborn and Derbyshire, 2010). Hence neuroscientists typically dichotomize and argue that pain empathy relies on sensory/embodied-simulation (Lamm et al., 2011) while the cognitive facet of empathy is missing except during explicit instructions for mentalization (Lamm et al., 2007; Fan and Han, 2008).

However, a recent neurophenomenological framework challenges the affective-cognitive dichotomy and suggests not to search for a single set of brain areas for a certain type of empathy but instead to examine the complex multi-rhythmicity in the cortex together with the individual’s subjective experiences such as social dynamics, lived encounters, and feedbacks (Levy and Bader, 2020).

They asserted that integrating subjective experiences with multi-faceted neuroscientific findings provides a more accurate and comprehensive outlook to describe the experience of empathy.

Thus far, the studies that looked into neural rhythms underlying empathy mainly reported the involvement of the alpha rhythm (Perry et al., 2010; Whitmarsh et al., 2011; Woodruff et al., 2011; Chen et al., 2012; Hoenen et al., 2015; Motoyama et al., 2017; Rieèanskı and Lamm, 2019). Alpha-band activity is involved in numerous emotional and cognitive processes (Klimesch et al., 2007; Hanslmayr et al., 2012; Bauer et al., 2014; Frey et al., 2015; Sadaghiani and Kleinschmidt, 2016; Schubring and Schupp, 2021), and in particular, it has a unique dual functionality: a cortical inhibitory control role reflected by an increase in alpha band power (i.e., enhancement) as well as an active role “gating by inhibition” (Jensen and Mazaheri, 2010). Accordingly, alpha power suppression is thought to reflect release from inhibition in the brain (Pfurtscheller and Lopes da Silva, 1999; Mazaheri et al., 2009; Haegens et al., 2010; Jensen and Mazaheri, 2010).

In addition to these multiple studies on the involvement of alpha suppression vs enhancement in cognition, a recent series of studies point to its involvement in affective processing of vicarious pain (Whitmarsh et al., 2011; Rieèanskı et al., 2015; Levy et al., 2018) and distress (Levy et al., 2016, 2019a,b, 2019c; Pratt et al., 2016) as well as inhibitory control in response to negative emotional stimuli (Schubring and Schupp, 2021).

Furthermore, there are other aspects of alpha rhythmicity which deserve attention: timing (e.g., early vs late) and phase-locking (e.g., induced vs evoked activity), just like other studies on working memory (Deiber et al., 2007) and emotion (Schubring and Schupp, 2021). In particular, while few studies examined induced neural response during empathy (Levy et al., 2016, 2018), induced activity reflects integrative functions, and not only externally-evoked processes and is therefore crucial not to overlook (Tallon-Baudry and Bertrand, 1999). Hence, the examination of the alpha rhythm during the process of empathy should not relate to alpha as a uni-dimensional phenomenon, but rather to multiple features such as suppression vs enhancement, timing and phase-locking.

Despite the almost exclusive focus on the role of the alpha rhythm in empathy, a few studies reported the involvement of the beta rhythm. However, none of these studies inspected the sources of beta activity in the brain and expounded the role of beta oscillations in empathetic responses (Whitmarsh et al., 2011; Rieèanskı et al., 2015; Levy et al., 2018). More broadly, the functional role of beta-band oscillations in cognitive and perceptual processing has been reviewed (Engel and Fries, 2010; Bressler and Richter, 2015), and it has been proposed that this rhythm is associated with the maintenance of the current processing or so-called “status quo.”

In other words, the modulation in beta-band power is thought to reflect the involvement in the top-down cognitive processing applied by an unexpected external stimulus. Hence, these converging lines of research emphasize the need for further investigation of the role that beta oscillations play during the experience of empathy and distinguishing its functional contribution from that of the alpha rhythm.

Notwithstanding the importance of inspecting complex neural rhythmicity, another crucial aspect is the subjective experience of empathy, or in other words, its phenomenological representation (Zahavi, 2012). By focusing on the subjective experience of empathy, phenomenological studies show that empathy is not dichotomous but rather a graded process (Stein, 1989; Fuchs, 2017). Recently, Grice-Jackson and colleagues demonstrated that the affective-cognitive dichotomy cannot straightforwardly accommodate neuroimaging representations of pain empathy that incorporate also its subjective representations (Grice-Jackson et al.,2017a,b). Specifically, the authors implemented a task [vicarious pain questionnaire (VPQ)] that presented vignettes of individuals in painful situations, and it inquired about the graded level of the subjective experience of self-pain while perceiving vicarious pain.

The main goal of the current study is to test whether pain empathy can be represented as a graded phenomenon, inspired by the Graded Empathy framework. Specifically, we test whether empathy can extend beyond the dichotomous view of embodied-simulation vs cognitive facets, and beyond the exclusive focus on distinct neural substrates (in neuroimaging studies) or on the alpha rhythm (in electrophysiological studies).

Hence, we examine the multiple rhythmic aspects of MEG signal during pain empathy by inspecting a broad frequency band, long time window, and induced activity. Moreover, we investigate the cortical generators of these brain oscillations (Baillet, 2017; Gross, 2019) to facilitate the interpretation of their functional role in pain empathy. We hypothesize that the multidimensional examination of neural patterns will reveal a multifaceted, rather than dichotomous, neural representation of pain empathy including sensory, affective, cognitive, bottom-up and top-down components.

Finally, we further examine the nature of the potential link between these neural representations and reports of subjective-experience and cognitive-affective traits. Specifically, we collect reports on subjective-experience during pain empathy (Grice-Jackson et al., 2017a) and on affective-cognitive traits (IRI; Davis, 1983), and test two predictions: that the brain-experience correspondence is either graded (i.e., as a function of subjective-experience rating) or dichotomous (i.e., functionally divided by affective-cognitive traits), thereby providing an additional examination of the graded vs the dichotomous frameworks.

reference link :https://www.frontiersin.org/articles/10.3389/fnhum.2021.708107/full

Original Research: Closed access.
Hemispherically lateralized rhythmic oscillations in the cingulate-amygdala circuit drive affective empathy in mice” by SHIN Hee-Sup et al. Neuron


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