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Dynamic pupillary exchange engages brain regions encoding social salience.

Harrison NA, Gray MA, Critchley HD - Soc Neurosci (2008)

Bottom Line: Discordance between observed and observer's pupillary changes enhanced activity within bilateral anterior insula, left amygdala and anterior cingulate.Our findings suggest pupillary signals are monitored continuously during social interactions and that incongruent changes activate brain regions involved in tracking motivational salience and attentionally meaningful information.Our data provide empirical evidence for an autonomically mediated extension of forward models of motor control into social interaction.

View Article: PubMed Central - PubMed

Affiliation: University College London, London, UK. n.harrison@fil.ion.ucl.ac.uk

ABSTRACT
Covert exchange of autonomic responses may shape social affective behavior, as observed in mirroring of pupillary responses during sadness processing. We examined how, independent of facial emotional expression, dynamic coherence between one's own and another's pupil size modulates regional brain activity. Fourteen subjects viewed pairs of eye stimuli while undergoing fMRI. Using continuous pupillometry biofeedback, the size of the observed pupils was varied, correlating positively or negatively with changes in participants' own pupils. Viewing both static and dynamic stimuli activated right fusiform gyrus. Observing dynamically changing pupils activated STS and amygdala, regions engaged by non-static and salient facial features. Discordance between observed and observer's pupillary changes enhanced activity within bilateral anterior insula, left amygdala and anterior cingulate. In contrast, processing positively correlated pupils enhanced activity within left frontal operculum. Our findings suggest pupillary signals are monitored continuously during social interactions and that incongruent changes activate brain regions involved in tracking motivational salience and attentionally meaningful information. Naturalistically, dynamic coherence in pupillary change follows fluctuations in ambient light. Correspondingly, in social contexts discordant pupil response is likely to reflect divergence of dispositional state. Our data provide empirical evidence for an autonomically mediated extension of forward models of motor control into social interaction.

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Related in: MedlinePlus

(A) Mean change in observer's pupil size preceding an observed pupil size change. (B) Mean change in observer's pupil size following an observed pupil size change. (C) Change in observer's pupils 2 frames (33 ms) after an observed change in pupil size. (D) Change in observer's pupils 3 frames (50 ms) after an observed change in pupil size.
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Figure 2: (A) Mean change in observer's pupil size preceding an observed pupil size change. (B) Mean change in observer's pupil size following an observed pupil size change. (C) Change in observer's pupils 2 frames (33 ms) after an observed change in pupil size. (D) Change in observer's pupils 3 frames (50 ms) after an observed change in pupil size.

Mentions: Analysis of subjects’ pupil data immediately preceding a change in observed pupil size confirmed that observed pupillary constrictions and dilations were preceded by congruent (positive feedback) and incongruent (negative feedback) pupillary changes in the observer, repeated measures ANOVA, interaction between factors feedback type (positive or negative) and pupillary change (constriction or dilation), F(1,13) = 190.2, p < .001 (Figure 2a). The mean change in subjects’ pupil size driving a change in the observed stimulus was 0.18 mm and did not differ between feedback conditions, paired t-test t(13) = 1.05, p = .31, or between constrictions or dilations, t(13) =−0.43, p = .67. There was also a significant interaction between feedback type and subjects’ pupillary response (dilation or constriction) immediately following an observed pupil size change, F(1, 13) = 66.6, p < .001 (Figure 2b). Interestingly, this showed the opposite interaction, i.e., rather than mimicking the observed pupil size change subjects’ pupils showed a small (mean 0.06 mm) constriction if the previous change was a dilation and vice versa. The direction of this effect argues against a direct mimetic response to the observed stimulus and, further, the timescale (< 17 ms) is too rapid for this or an effect driven by the pupillary light reflex (latency ~ 180 ms). Again there was no significant difference in the size of this pupillary response between feedback types (p = .88) or between constrictions or dilations (p = .72). Change in observed stimuli did not have a significant effect on subjects’ subsequent pupillary responses (Figure 2c and 2d). Together this suggests a compensatory constriction following a previous dilation and vice versa that is not influenced by feedback condition.


Dynamic pupillary exchange engages brain regions encoding social salience.

Harrison NA, Gray MA, Critchley HD - Soc Neurosci (2008)

(A) Mean change in observer's pupil size preceding an observed pupil size change. (B) Mean change in observer's pupil size following an observed pupil size change. (C) Change in observer's pupils 2 frames (33 ms) after an observed change in pupil size. (D) Change in observer's pupils 3 frames (50 ms) after an observed change in pupil size.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2913324&req=5

Figure 2: (A) Mean change in observer's pupil size preceding an observed pupil size change. (B) Mean change in observer's pupil size following an observed pupil size change. (C) Change in observer's pupils 2 frames (33 ms) after an observed change in pupil size. (D) Change in observer's pupils 3 frames (50 ms) after an observed change in pupil size.
Mentions: Analysis of subjects’ pupil data immediately preceding a change in observed pupil size confirmed that observed pupillary constrictions and dilations were preceded by congruent (positive feedback) and incongruent (negative feedback) pupillary changes in the observer, repeated measures ANOVA, interaction between factors feedback type (positive or negative) and pupillary change (constriction or dilation), F(1,13) = 190.2, p < .001 (Figure 2a). The mean change in subjects’ pupil size driving a change in the observed stimulus was 0.18 mm and did not differ between feedback conditions, paired t-test t(13) = 1.05, p = .31, or between constrictions or dilations, t(13) =−0.43, p = .67. There was also a significant interaction between feedback type and subjects’ pupillary response (dilation or constriction) immediately following an observed pupil size change, F(1, 13) = 66.6, p < .001 (Figure 2b). Interestingly, this showed the opposite interaction, i.e., rather than mimicking the observed pupil size change subjects’ pupils showed a small (mean 0.06 mm) constriction if the previous change was a dilation and vice versa. The direction of this effect argues against a direct mimetic response to the observed stimulus and, further, the timescale (< 17 ms) is too rapid for this or an effect driven by the pupillary light reflex (latency ~ 180 ms). Again there was no significant difference in the size of this pupillary response between feedback types (p = .88) or between constrictions or dilations (p = .72). Change in observed stimuli did not have a significant effect on subjects’ subsequent pupillary responses (Figure 2c and 2d). Together this suggests a compensatory constriction following a previous dilation and vice versa that is not influenced by feedback condition.

Bottom Line: Discordance between observed and observer's pupillary changes enhanced activity within bilateral anterior insula, left amygdala and anterior cingulate.Our findings suggest pupillary signals are monitored continuously during social interactions and that incongruent changes activate brain regions involved in tracking motivational salience and attentionally meaningful information.Our data provide empirical evidence for an autonomically mediated extension of forward models of motor control into social interaction.

View Article: PubMed Central - PubMed

Affiliation: University College London, London, UK. n.harrison@fil.ion.ucl.ac.uk

ABSTRACT
Covert exchange of autonomic responses may shape social affective behavior, as observed in mirroring of pupillary responses during sadness processing. We examined how, independent of facial emotional expression, dynamic coherence between one's own and another's pupil size modulates regional brain activity. Fourteen subjects viewed pairs of eye stimuli while undergoing fMRI. Using continuous pupillometry biofeedback, the size of the observed pupils was varied, correlating positively or negatively with changes in participants' own pupils. Viewing both static and dynamic stimuli activated right fusiform gyrus. Observing dynamically changing pupils activated STS and amygdala, regions engaged by non-static and salient facial features. Discordance between observed and observer's pupillary changes enhanced activity within bilateral anterior insula, left amygdala and anterior cingulate. In contrast, processing positively correlated pupils enhanced activity within left frontal operculum. Our findings suggest pupillary signals are monitored continuously during social interactions and that incongruent changes activate brain regions involved in tracking motivational salience and attentionally meaningful information. Naturalistically, dynamic coherence in pupillary change follows fluctuations in ambient light. Correspondingly, in social contexts discordant pupil response is likely to reflect divergence of dispositional state. Our data provide empirical evidence for an autonomically mediated extension of forward models of motor control into social interaction.

Show MeSH
Related in: MedlinePlus