Sensorimotor Alpha Activity is Modulated in Response to the Observation of Pain in Others

Abstract

The perception–action account of empathy states that observation of another person's state automatically activates a similar state in the observer. It is still unclear in what way ongoing sensorimotor alpha oscillations are involved in this process. Although they have been repeatedly implicated in (biological) action observation and understanding communicative gestures, less is known about their role in vicarious pain observation. Their role is understood as providing a graded inhibition through functional inhibition, thereby streamlining information flow through the cortex. Although alpha oscillations have been shown to have at least visual and sensorimotor origins, only the latter are expected to be involved in the empathetic response. Here, we used magnetoencephalography, allowing us to spatially distinguish and localize oscillatory components using beamformer source reconstruction. Subjects observed realistic pictures of limbs in painful and no-pain (control) conditions. As predicted, time–frequency analysis indeed showed increased alpha suppression in the pain condition compared to the no-pain condition. Although both pain and no-pain conditions suppressed alpha- and beta-band activity at both posterior and central sensors, the pain condition suppressed alpha more only at central sensors. Source reconstruction localized these differences along the central sulcus. Our results could not be accounted for by differences in the evoked fields, suggesting a unique role of oscillatory activity in empathetic responses. We argue that alpha oscillations provide a unique measure of the underlying functional architecture of the brain, suggesting an automatic disinhibition of the sensorimotor cortices in response to the observation of pain in others.

Prior exposure to extreme pain alters neural response to pain in others

“…The findings are also compatible with previous E/MEG studies showing that early responses to others' pain can be observed within 200 ms following stimulus onset (Cheng et al, 2008;. In addition, our findings are in line with those from previous studies on the perception of others' pain that have shown activation in regions of the cingulate (Höfle et al, 2013) and sensorimotor (Cheng et al, 2008;Whitmarsh et al, 2011) cortices, as well as in posterior brain regions, including the FG (Höfle et al, 2013;Singer et al, 2004). Finally, similar to previous reports, we found a Bpain effect^also in the STG (Botvinick et al, 2005;Singer et al, 2004), a region associated with salience (Hayes, Hayes, & Mikedis, 2012;White, Joseph, Francis, & Liddle, 2010) and social information processing (Bernhardt & Singer, 2012), which was extended to the posterior insula, which is known to be associated with the sensory experience of pain (Peyron et al, 2000;Sabatini et al, 2009).…”

“…Consistent with previous studies of pain perception (Cheng et al, 2008;Whitmarsh et al, 2011) and the attention-drawing nature of survival-related stimuli (Bradley, 2009), we found a Bpain effect^in the control group marked by significantly greater alpha suppression in the painful than in the neutral condition in the PCC. This pattern, which may reflect enhanced evaluation of the more important stimulus (i.e., pain), was altered in the pain-exposed group, suggesting that prior exposure to severe pain in others is associated with alterations to the neural response to pain-related stimuli in specific brain areas.…”

“…These studies have demonstrated that observing pain in others induces modulations in oscillatory brain activity in the alpha frequency range (8-12 Hz; Cheng et al, 2008;Mu, Fan, Mao, & Han, 2008;Perry, Bentin, Bartal, Lamm, & Decety, 2010;Whitmarsh, Nieuwenhuis, Barendregt, & Jensen, 2011;Yang, Decety, Lee, Chen, & Cheng, 2009). Oscillatory alpha activity is the predominant frequency in humans during rest and is suppressed in brain regions while processing relevant sensory information (Jensen & Mazaheri, 2010;Klimesch, 2012).…”

“…When recorded over sensorimotor cortices, alpha oscillations are termed mu oscillations (Kuhlman, 1978). Two MEG studies (Cheng et al, 2008;Whitmarsh et al, 2011) showed mu suppression in responses to body parts in painful and nonpainful situations, which was significantly stronger in the pain condition. Comparable results have been found in EEG studies (Perry et al, 2010;Yang et al, 2009; but see Mu et al, 2008) using similar stimuli.…”

Oxytocin selectively modulates brain response to stimuli probing social synchrony

“…Alpha rhythm functions through inhibition; an alpha oscillatory increase reflects suppressed cortical reactivity whereas alpha oscillatory suppression indexes enhanced reactivity and cortical recruitment (for a review, Jensen and Mazaheri, 2010). Evidence highlights the role of alpha rhythms in supporting social functions (Whitmarsh et al, 2011), biological motion (Ulloa and Pineda, 2007), and inter-individual synchronized actions (Dumas et al, 2010). Furthermore, EEG research showed that OT regulates alpha rhythms during social processing, possibly via modulation of MNS (Perry et al, 2010).…”