Dynamics of aesthetic experience are reflected in the default-mode network

Abstract

Neuroaesthetics is a rapidly developing interdisciplinary field of research that aims to understand the neural substrates of aesthetic experience: While understanding aesthetic experience has been an objective of philosophers for centuries, it has only more recently been embraced by neuroscientists. Recent work in neuroaesthetics has revealed that aesthetic experience with static visual art engages visual, reward and default-mode networks. Very little is known about the temporal dynamics of these networks during aesthetic appreciation. Previous behavioral and brain imaging research suggests that critical aspects of aesthetic experience have slow dynamics, taking more than a few seconds, making them amenable to study with fMRI. Here, we identified key aspects of the dynamics of aesthetic experience while viewing art for various durations. In the first few seconds following image onset, activity in the DMN (and high-level visual and reward regions) was greater for very pleasing images; in the DMN this activity counteracted a suppressive effect that grew longer and deeper with increasing image duration. In addition, for very pleasing art, the DMN response returned to baseline in a manner time-locked to image offset. Conversely, for non-pleasing art, the timing of this return to baseline was inconsistent. This differential response in the DMN may therefore reflect the internal dynamics of the participant's state: The participant disengages from art-related processing and returns to stimulus-independent thought. These dynamics suggest that the DMN tracks the internal state of a participant during aesthetic experience.

Figure 1.. Stimuli and trial structure.

A. Examples of stimuli. B. Depiction of trial structure. Trials consisted of a 1 s fixation cross, followed by stimulus presentation for either 1, 5, or 15 s. At stimulus onset, participants began continuously rating their pleasure using an fMRI-compatible squeezeball. After stimulus offset, participants continued rating their pleasure during a 14 s post-stimulus period. Following this post-stimulus period, participants had 4 s to make an overall rating of the stimulus between low (L) and high (H) using a track ball held in the opposite hand.

Figure 2.. Continuous pleasure responses.

A-C) Average pleasure over time for high (green), medium (blue), and low (red) rated trials; colored shaded areas represent ±1 standard error of the mean (SEM). Black lines represent model fits. Gray shaded areas represent time windows during which the stimulus was present. Each panel shows data for one duration: 1 s (a), 5 s (b), and 15 s (c). D) Average pleasure amplitude r_steady per condition. Error bars represent ± SEM. All differences between ratings or durations are at least marginally significant, p < 0.066, unless otherwise indicated.

Figure 3.. Effects of aesthetic appreciation in large-scale brain networks.

Trial-triggered average BOLD signal extracted from three large-scale brain networks: The default-mode network (DMN), the basal ganglia, and a lateral visual network (consisting of lateral occipitotemporal, ventral occipitotemporal, and parietal visual regions). For each network, the first row illustrates the response to low-rated trials (red), and the second row illustrates the difference between responses to high vs. low (green) and medium vs. low (blue) trials. Gray shading indicates image presentation (duration of 1, 5 or 15 s). The DMN and lateral visual networks were identified by correlating individual-participant ICA maps derived from a rest scan with published network maps (Smith et al., 2009). Color shaded areas indicate ±1 SEM. *Indicates significant differences between high and low trials. †Indicates significant differences between high trials vs. medium and low trials.

Figure 4.. Differential sensitivity in subregions of the DMN to aesthetic appreciation.

For each region, the first row illustrates the response to low-rated trials (red), and the second row illustrates the difference between responses to high vs. low (green) and medium vs. low (blue) trials. Gray shading indicates image presentation (duration of 1, 5 or 15 s). Regions were extracted by combining individual-participant DMN maps with subregion masks defined in a common (Freesurfer fsaverage) surface space. Color shaded areas indicate ±1 SEM. *Indicates significant differences between high and low trials. †Indicates significant differences between high trials vs. medium and low trials.

Figure 5.. Differential sensitivity of basal-ganglia subregions to aesthetic appreciation.

For each region, the first row illustrates the response to low-rated trials (red), and the second row illustrates the difference between responses to high vs. low (green) and medium vs. low (blue) trials. Gray shading indicates image presentation (duration of 1, 5 or 15 s). ROIs were created from an automatic volumetric segmentation of individual participant high-resolution T1 scans (Freesurfer aseg). Color shaded areas indicate ±1 SEM. *Indicates significant differences between high and low trials. †Indicates significant differences between high trials vs. medium and low trials. ‡Indicates significant differences between low vs. high and medium trials. §Indicates significant differences between low and medium trials.

Figure 6.. DMN shows a response locked to stimulus offset for only high-rated trials.

DMN responses aligned by offset for low (left) medium (middle) and high-rated trials (right). Darkest colors depict 1 s trials, medium colors depict 5 s trials, and brightest colors depict 15 s trials. Red arrow depicts timepoint at which BOLD signal returns to baseline simultaneously for all three trial durations; this is not present in low and medium-rated trials.