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A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers' perspective.

ABSTRACT: Empathy relies on brain systems that support the interaction between an observer's mental state and cues about the others' experience. Beyond the core brain areas typically activated in pain empathy studies (insular and anterior cingulate cortices), the diversity of paradigms used may reveal secondary networks that subserve other more specific processes. A coordinate-based meta-analysis of fMRI experiments on pain empathy was conducted to obtain activation likelihood estimates along three factors and seven conditions: visual cues (body parts, facial expressions), visuospatial (first-person, thirdperson), and cognitive (self-, stimuli-, other-oriented tasks) perspectives. The core network was found across cues and perspectives, and common activation was observed in higher-order visual areas. Body-parts distinctly activated areas related with sensorimotor processing (superior and inferior parietal lobules, anterior insula) while facial expression distinctly involved the inferior frontal gyrus. Self- compared to other-perspective produced distinct activations in the left insula while stimulus- versus other-perspective produced distinctive responses in the inferior frontal and parietal lobules, precentral gyrus, and cerebellum. Pain empathy relies on a core network which is modulated by several secondary networks. The involvement of the latter seems to depend on the visual cues available and the observer's mental state that can be influenced by specific instructions.

SUBMITTER: Jauniaux J

PROVIDER: S-EPMC6847411 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers' perspective.

Jauniaux Josiane J Khatibi Ali A Rainville Pierre P Jackson Philip L PL

Social cognitive and affective neuroscience 20190801 8

Empathy relies on brain systems that support the interaction between an observer's mental state and cues about the others' experience. Beyond the core brain areas typically activated in pain empathy studies (insular and anterior cingulate cortices), the diversity of paradigms used may reveal secondary networks that subserve other more specific processes. A coordinate-based meta-analysis of fMRI experiments on pain empathy was conducted to obtain activation likelihood estimates along three factor ...[more]

PMID: 31393982

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Project description:Empathy is an essential component of our social lives, allowing us to understand and share other people's affective and sensory states, including pain. Evidence suggests a core neural network-including anterior insula (AI) and mid-cingulate cortex (MCC)-is involved in empathy for pain. However, a similar network is associated to empathy for non-pain affective states, raising the question whether empathy for pain is unique in its neural correlates. Furthermore, it is yet unclear whether neural correlates converge across different stimuli and paradigms that evoke pain-empathy. We performed a coordinate-based activation likelihood estimation (ALE) meta-analysis to identify neural correlates of empathy, assess commonalities and differences between empathy for pain and for non-pain negative affective states, and differences between pain-empathy evoking stimuli (i.e., facial pain expressions vs. acute pain inflictions) and paradigms (i.e., perceptual/affective vs. cognitive/evaluative paradigms). Following a systematic search, data from 128 functional brain imaging studies presenting whole-brain results of an empathy condition vs. baseline/neutral condition were extracted. Synthesizing neural correlates of empathy confirmed a core network comprising AI, MCC, postcentral gyrus, inferior parietal lobe, thalamus, amygdala, and brainstem. There was considerable overlap in networks for empathy for pain and empathy for non-pain negative affective states. Important differences also arose: empathy for pain uniquely activated bilateral mid-insula and more extensive MCC. Regarding stimuli, painful faces and acute pain inflictions both evoked the core empathy regions, although acute pain inflictions activated additional regions including medial frontal and parietal cortex. Regarding paradigms, both perceptual/affective and cognitive/evaluative paradigms recruited similar neural circuitry, although cognitive/evaluative paradigms activated more left MCC regions while perceptual/affective paradigms activated more right AI. Taken together, our findings reveal that empathy for pain and empathy for non-pain negative affective states share considerable neural correlates, particularly in core empathy regions AI and MCC. Beyond these regions, important differences emerged, limiting generalizability of findings across different affective/sensory states. Within pain-empathy studies, the core regions were recruited robustly irrespective of stimuli or instructions, allowing one to tailor designs according to specific needs to some extent, while ensuring activation of core regions.

Project description:BackgroundNeural decoding could be useful in many ways, from serving as a neuroscience research tool to providing a means of augmented communication for patients with neurological conditions. However, applications of decoding are currently constrained by the limitations of traditional neuroimaging modalities. Electrocorticography requires invasive neurosurgery, magnetic resonance imaging (MRI) is too cumbersome for uses like daily communication, and alternatives like functional near-infrared spectroscopy (fNIRS) offer poor image quality. High-density diffuse optical tomography (HD-DOT) is an emerging modality that uses denser optode arrays than fNIRS to combine logistical advantages of optical neuroimaging with enhanced image quality. Despite the resulting promise of HD-DOT for facilitating field applications of neuroimaging, decoding of brain activity as measured by HD-DOT has yet to be evaluated.ObjectiveTo assess the feasibility and performance of decoding with HD-DOT in visual cortex.Methods and resultsTo establish the feasibility of decoding at the single-trial level with HD-DOT, a template matching strategy was used to decode visual stimulus position. A receiver operating characteristic (ROC) analysis was used to quantify the sensitivity, specificity, and reproducibility of binary visual decoding. Mean areas under the curve (AUCs) greater than 0.97 across 10 imaging sessions in a highly sampled participant were observed. ROC analyses of decoding across 5 participants established both reproducibility in multiple individuals and the feasibility of inter-individual decoding (mean AUCs > 0.7), although decoding performance varied between individuals. Phase-encoded checkerboard stimuli were used to assess more complex, non-binary decoding with HD-DOT. Across 3 highly sampled participants, the phase of a 60° wide checkerboard wedge rotating 10° per second through 360° was decoded with a within-participant error of 25.8±24.7°. Decoding between participants was also feasible based on permutation-based significance testing.ConclusionsVisual stimulus information can be decoded accurately, reproducibly, and across a range of detail (for both binary and non-binary outcomes) at the single-trial level (without needing to block-average test data) using HD-DOT data. These results lay the foundation for future studies of more complex decoding with HD-DOT and applications in clinical populations.

Dataset Information

A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers' perspective.

Publications

A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers' perspective.

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