Research Article: Modulation of neural circuits underlying temporal production by facial expressions of pain

Date Published: February 15, 2018

Publisher: Public Library of Science

Author(s): Daniela Ballotta, Fausta Lui, Carlo Adolfo Porro, Paolo Frigio Nichelli, Francesca Benuzzi, Cosimo Urgesi.

http://doi.org/10.1371/journal.pone.0193100

Abstract

According to the Scalar Expectancy Theory, humans are equipped with a biological internal clock, possibly modulated by attention and arousal. Both emotions and pain are arousing and can absorb attentional resources, thus causing distortions of temporal perception. The aims of the present single-event fMRI study were to investigate: a) whether observation of facial expressions of pain interferes with time production; and b) the neural network subserving this kind of temporal distortions. Thirty healthy volunteers took part in the study. Subjects were asked to perform a temporal production task and a concurrent gender discrimination task, while viewing faces of unknown people with either pain-related or neutral expressions. Behavioural data showed temporal underestimation (i.e., longer produced intervals) during implicit pain expression processing; this was accompanied by increased activity of right middle temporal gyrus, a region known to be active during the perception of emotional and painful faces. Psycho-Physiological Interaction analyses showed that: 1) the activity of middle temporal gyrus was positively related to that of areas previously reported to play a role in timing: left primary motor cortex, middle cingulate cortex, supplementary motor area, right anterior insula, inferior frontal gyrus, bilateral cerebellum and basal ganglia; 2) the functional connectivity of supplementary motor area with several frontal regions, anterior cingulate cortex and right angular gyrus was correlated to the produced interval during painful expression processing. Our data support the hypothesis that observing emotional expressions distorts subjective time perception through the interaction of the neural network subserving processing of facial expressions with the brain network involved in timing. Within this frame, middle temporal gyrus appears to be the key region of the interplay between the two neural systems.

Partial Text

Time processing is crucial for every-day life and is flexibly modulated by ongoing experiences. The temporal perception literature shows that emotions are one of the most significant sources of temporal distortion. Different types of emotional stimuli, such as affective images [1–4], fear-inducing stimuli [5] and emotional sounds [6], have been used to investigate the mechanisms underlying emotional modulation of subjective time experience. In particular, consistent findings have been obtained using emotional facial expressions [7,8]: fearful, angry, happy and sad expressions were perceived as lasting longer than neutral expressions presented for the same duration.

The main results of this study were as follows: a) as expected, the concurrent gender discrimination task interferes with temporal production [29], causing underestimation of time intervals (namely, participants produced longer intervals); the underestimation was significantly higher when observing facial expressions of pain, as compared to neutral expressions; b) the implicit observation of pain expressions during time production modulated activity in the right MTG; c) functional connectivity between SMA and several cortical regions was correlated to the produced time interval during painful facial expression processing; d) neural activity of right MTG was positively related to the activity of regions belonging to the timing network, whereas it was negatively related to the activity of cortical regions involved in temporal decision making and in processing pain-related information.

The present study provides the first evidence that observation of facial expressions of pain interact with timing at the behavioral and neural level. The right posterior MTG appears to be the key region mediating the interaction between the brain network analyzing painful expressions and the neural network involved in timing.

 

Source:

http://doi.org/10.1371/journal.pone.0193100

 

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