Neural correlates of the affective properties of spontaneous and volitional laughter types

Abstract

Previous investigations of vocal expressions of emotion have identified acoustic and perceptual distinctions between expressions of different emotion categories, and between spontaneous and volitional (or acted) variants of a given category. Recent work on laughter has identified relationships between acoustic properties of laughs and their perceived affective properties (arousal and valence) that are similar across spontaneous and volitional types (Bryant & Aktipis, 2014; Lavan et al., 2016). In the current study, we explored the neural correlates of such relationships by measuring modulations of the BOLD response in the presence of itemwise variability in the subjective affective properties of spontaneous and volitional laughter. Across all laughs, and within spontaneous and volitional sets, we consistently observed linear increases in the response of bilateral auditory cortices (including Heschl's gyrus and superior temporal gyrus [STG]) associated with higher ratings of perceived arousal, valence and authenticity. Areas in the anterior medial prefrontal cortex (amPFC) showed negative linear correlations with valence and authenticity ratings across the full set of spontaneous and volitional laughs; in line with previous research (McGettigan et al., 2015; Szameitat et al., 2010), we suggest that this reflects increased engagement of these regions in response to laughter of greater social ambiguity. Strikingly, an investigation of higher-order relationships between the entire laughter set and the neural response revealed a positive quadratic profile of the BOLD response in right-dominant STG (extending onto the dorsal bank of the STS), where this region responded most strongly to laughs rated at the extremes of the authenticity scale. While previous studies claimed a role for right STG in bipolar representation of emotional valence, we instead argue that this may in fact exhibit a relatively categorical response to emotional signals, whether positive or negative.

Keywords: Affective properties; FMRI; Laughter; Parametric modulations; Perception.

Figure 1

a-c. Scatterplots showing the relationships between ratings of arousal, valence and authenticity for spontaneous and volitional laughs (including within-set linear trendlines).

Figure 2

Regions showing significant positive (green) and negative (red) linear relationships between the BOLD response and affective properties of laughter, across all spontaneous and volitional laughs, for a) arousal, b) valence, c) authenticity. Results are shown at a voxel height threshold of p < .005 (uncorrected), and a corrected cluster threshold of p < .001 (Slotnick et al., 2003). Bar plots show the linear trend between affective ratings and percent signal change in the peak STG voxels.

Figure 3

Regions showing significant quadratic relationships between the BOLD response and affective properties of laughter, across all spontaneous and volitional laughs, for a) arousal, b) valence, c) authenticity. Results are shown at a voxel height threshold of p < .005 (uncorrected), and a corrected cluster threshold of p < .001 (Slotnick et al., 2003). Bar plots show the quadratic trends between affective ratings and percent signal change in the peak voxels for each analysis.

Figure 4

Regions showing positive linear (magenta) and positive quadratic (yellow) trends in the correlation of the BOLD signal with a) valence ratings and b) authenticity ratings. Regions in white indicate overlap of the two effects. Results are shown at a voxel height threshold of p < .005 (uncorrected), and a corrected cluster threshold of p < .001 (Slotnick et al., 2003).

Figure 5

Regions showing significant positive linear relationships between the BOLD response and affective properties of spontaneous (red) and volitional (blue) laughter, for a) arousal, b) valence, c) authenticity. Overlap is shown in magenta. Results are shown at a voxel height threshold of p < .005 (uncorrected), and a corrected cluster threshold of p < .001 (Slotnick et al., 2003).