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Double dissociation of neural responses supporting perceptual and cognitive components of social cognition: evidence from processing of others' pain.

Sessa P, Meconi F, Han S - Sci Rep (2014)

Bottom Line: In the context of the neuroscience of empathy analogous systems have been described.Notably, the reactions to pain triggered by these cues added up when both were available, that is the joint reaction was characterized by additive effects.These findings favor a model assuming distinct neural paths of perceptual and cognitive processing, at least when the cognitive component is triggered by language.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Developmental and Social Psychology, University of Padova, Padova, Italy [2] Centre for Cognitive Neuroscience, University of Padova, Padova, Italy.

ABSTRACT
Models on how perceptual and cognitive information on others' mental states are treated by the cognitive architecture are often framed as duplex models considering two independent systems. In the context of the neuroscience of empathy analogous systems have been described. Using event-related potentials (i.e., ERPs) technique, we tested the hypothesis of temporal dissociation of two functional systems. We implemented a design in which perceptual (i.e., painful or neutral facial expressions) and contextual (i.e., painful or neutral related sentences) cues on others' mental states were orthogonally manipulated. Painful expressions selectively modulated the early activity at 110-360 ms over fronto-central and centro-parietal regions, whereas painful contexts selectively modulated the late activity at 400-840 ms over these same regions. Notably, the reactions to pain triggered by these cues added up when both were available, that is the joint reaction was characterized by additive effects. These findings favor a model assuming distinct neural paths of perceptual and cognitive processing, at least when the cognitive component is triggered by language.

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Timeline and conditions in the present experiment.
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f1: Timeline and conditions in the present experiment.

Mentions: Although the excellent spatial resolution of fMRI allowed localization of plausible neural underpinnings of experience sharing and mentalizing, its poor temporal resolution did not assist in deploying processing within the two streams in the temporal domain so that it is still unclear if and when a functional interplay between them occurs. For instance, it is unclear whether this functional interplay may occur for verbal information (e.g., description of an accident) coherent with an observed scene (e.g., painful face). By recording event-related potentials (ERPs), we tested the hypothesis of temporal and functional dissociations between perceptual and contextual routes of social cognition during empathy for others' pain. We implemented a design in which perceptual (i.e., pictures of faces with either painful or neutral expressions) and contextual information (i.e., sentences describing either a painful or neutral contexts) were orthogonally manipulated (see Figure 1). The domain of language is strictly related to the cognitive component of social cognition and ToM33334353637 and strong evidence supporting this claim comes from studies on deaf children who usually present delays in reasoning about intentions and desires383940414243. In this vein, the contextual information provided by sentences in the present study would require high level cognitive processing. Participants had to decide whether the face had a neutral or a painful expression by pressing one of two response keys and they were required to rate their subjective impression of empathy capability for each presented context/face. Three possible neural reactions to others' pain were monitored: perception-based reaction (a modulation of ERPs as a function of facial expressions), context-based reaction (a modulation of ERPs as a function of verbal information), and joint reaction (a modulation of ERPs as a function of both facial expressions and verbal information). At least, two alternative empirical scenarios were expected, supporting two distinct models. According to a model assuming distinct neural paths of perceptual and cognitive processing, modulations associated with the two cue categories, either perceptual and contextual, would have been selectively confined to different time windows of the ERP waveforms, i.e., perception-based and context-based reactions would have been dissociated in time; within this empirical scenario, the complete dissociation of the two systems would manifest as additive effects of perception-based and context-based reactions when both cues are available (i.e., when both facial expression and context show painful information). On the contrary, the other empirical scenario favoring the functional interplay of the two cues and systems would have revealed as interactive effects of them, demonstrating that contextual information designating others' pain may boost processing of painful facial expressions and/or that painful facial expressions may enhance processing of contextual information. The former of the two hypothesized empirical scenarios would also provide more substantial evidence in favor of a two-system model, since it would strongly suggest that the two systems operate independently of each other, and that neither system interacts with the other system9.


Double dissociation of neural responses supporting perceptual and cognitive components of social cognition: evidence from processing of others' pain.

Sessa P, Meconi F, Han S - Sci Rep (2014)

Timeline and conditions in the present experiment.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4262888&req=5

f1: Timeline and conditions in the present experiment.
Mentions: Although the excellent spatial resolution of fMRI allowed localization of plausible neural underpinnings of experience sharing and mentalizing, its poor temporal resolution did not assist in deploying processing within the two streams in the temporal domain so that it is still unclear if and when a functional interplay between them occurs. For instance, it is unclear whether this functional interplay may occur for verbal information (e.g., description of an accident) coherent with an observed scene (e.g., painful face). By recording event-related potentials (ERPs), we tested the hypothesis of temporal and functional dissociations between perceptual and contextual routes of social cognition during empathy for others' pain. We implemented a design in which perceptual (i.e., pictures of faces with either painful or neutral expressions) and contextual information (i.e., sentences describing either a painful or neutral contexts) were orthogonally manipulated (see Figure 1). The domain of language is strictly related to the cognitive component of social cognition and ToM33334353637 and strong evidence supporting this claim comes from studies on deaf children who usually present delays in reasoning about intentions and desires383940414243. In this vein, the contextual information provided by sentences in the present study would require high level cognitive processing. Participants had to decide whether the face had a neutral or a painful expression by pressing one of two response keys and they were required to rate their subjective impression of empathy capability for each presented context/face. Three possible neural reactions to others' pain were monitored: perception-based reaction (a modulation of ERPs as a function of facial expressions), context-based reaction (a modulation of ERPs as a function of verbal information), and joint reaction (a modulation of ERPs as a function of both facial expressions and verbal information). At least, two alternative empirical scenarios were expected, supporting two distinct models. According to a model assuming distinct neural paths of perceptual and cognitive processing, modulations associated with the two cue categories, either perceptual and contextual, would have been selectively confined to different time windows of the ERP waveforms, i.e., perception-based and context-based reactions would have been dissociated in time; within this empirical scenario, the complete dissociation of the two systems would manifest as additive effects of perception-based and context-based reactions when both cues are available (i.e., when both facial expression and context show painful information). On the contrary, the other empirical scenario favoring the functional interplay of the two cues and systems would have revealed as interactive effects of them, demonstrating that contextual information designating others' pain may boost processing of painful facial expressions and/or that painful facial expressions may enhance processing of contextual information. The former of the two hypothesized empirical scenarios would also provide more substantial evidence in favor of a two-system model, since it would strongly suggest that the two systems operate independently of each other, and that neither system interacts with the other system9.

Bottom Line: In the context of the neuroscience of empathy analogous systems have been described.Notably, the reactions to pain triggered by these cues added up when both were available, that is the joint reaction was characterized by additive effects.These findings favor a model assuming distinct neural paths of perceptual and cognitive processing, at least when the cognitive component is triggered by language.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Developmental and Social Psychology, University of Padova, Padova, Italy [2] Centre for Cognitive Neuroscience, University of Padova, Padova, Italy.

ABSTRACT
Models on how perceptual and cognitive information on others' mental states are treated by the cognitive architecture are often framed as duplex models considering two independent systems. In the context of the neuroscience of empathy analogous systems have been described. Using event-related potentials (i.e., ERPs) technique, we tested the hypothesis of temporal dissociation of two functional systems. We implemented a design in which perceptual (i.e., painful or neutral facial expressions) and contextual (i.e., painful or neutral related sentences) cues on others' mental states were orthogonally manipulated. Painful expressions selectively modulated the early activity at 110-360 ms over fronto-central and centro-parietal regions, whereas painful contexts selectively modulated the late activity at 400-840 ms over these same regions. Notably, the reactions to pain triggered by these cues added up when both were available, that is the joint reaction was characterized by additive effects. These findings favor a model assuming distinct neural paths of perceptual and cognitive processing, at least when the cognitive component is triggered by language.

Show MeSH
Related in: MedlinePlus