Afferent cardiac signals modulate attentional engagement to low spatial frequency fearful faces

Abstract

Despite the growing consensus that the continuous dynamic cortical representations of internal bodily states shape the subjective experience of emotions, physiological arousal is typically considered only a consequence and rarely a determinant of the emotional experience. Recent experimental approaches study how afferent autonomic signals from the heart modulate the processing of sensory information by focussing on the phasic properties of arterial baroreceptor firing that is active during cardiac systole and quiescent during cardiac diastole. For example, baroreceptor activation has been shown to enhance the processing of threat-signalling stimuli. Here, we investigate the role of cardiac afferent signals in the rapid engagement and disengagement of attention to fear stimuli. In an adapted version of the emotional attentional cueing paradigm, we timed the presentation of cues, either fearful or neutral faces, to coincide with the different phases of the cardiac cycle. Moreover, we presented cues with different spatial frequency ranges to investigate how these interoceptive signals influence the processing of visual information. Results revealed a selective enhancement of attentional engagement to low spatial frequency fearful faces presented during cardiac systole relative to diastole. No cardiac cycle effects were observed to high spatial frequency nor broad spatial frequency cues. These findings expand our mechanistic understanding of how body-brain interactions may impact the visual processing of fearful stimuli and contribute to the increased attentional capture of threat signals.

The heart of cognitive control: Cardiac phase modulates processing speed and inhibition

“…Simple reaction time, a measure of processing speed (and a general index of “fluid” intelligence; Jakobsen, Sorensen, Rask, Jensen, & Kondrup, ; Sheppard & Vernon, ; Woods, Wyma, Yund, Herron, & Reed, ), can be considered as part of cognitive control (Koechlin et al, ). This result could be related to findings reporting a facilitated processing of visual stimuli during systole (Pramme, Larra, Schächinger, & Frings, ), such as low‐frequency fearful faces (Azevedo, Badoud, & Tsakiris, ). Taken together, these results tend to be coherent with the underlying neuroanatomical pathways of baroreceptor signal central integration.…”

Active information sampling varies across the cardiac cycle

“…Although in our study stimulus content was largely matched along several dimensions (physical image statistics and more high-level features), differences in stimulus features may still account for variation in memory effects associated with the cardiac cycle. For example, differences have been reported for different stimulus categories like words (Garfinkel et al, 2013), faces (Fiacconi et al, 2016), and complex scenes (present study), but also for low-level stimulus properties such as spatial frequency (Azevedo et al, 2018). However, accounting for picture as random effect in our GLMM analyses did not explain additional variance in memory performance across the cardiac cycle.…”

“…We studied the association between the cardiac cycle and self-paced visual sampling as well as visual recognition memory for pictures of different emotional valence. We hypothesized that facilitated visual processing (Pramme et al, 2014(Pramme et al, , 2016)-observed specifically for relevant or emotionally salient stimuli (Azevedo et al, 2018(Azevedo et al, , 2017Garfinkel et al, 2014)-as well as facilitated oculomotor processing during systole (Ohl et al, 2016) guides active perception in the shape of a preference to prompt a relevant visual stimulus during early phases of the cardiac cycle. We observed a significant accumulation of key presses (i.e., prompted picture onsets) during systole, thereby showing for the first time a coupling between self-paced visual sampling and the heartbeat.…”

“…To investigate perception and action within a comprehensive framework of mind-brain-body interactions, we studied cardiac-related sensorimotor processing in a self-paced visual sampling paradigm, in which participants decide when to press a key to see a task-relevant visual stimulus. Extending studies that emphasize a selectivity of this effect for motivationally salient, passively presented stimuli (Azevedo et al, 2018(Azevedo et al, , 2017Garfinkel et al, 2014), we predicted that observers implicitly act upon a relevant visual stimulus such that it is received (and perceived) during preferred cardiac phases. More specifically, we hypothesized that visual sampling would be biased toward processing taskrelevant pictures during systole.…”

“…Based on findings of facilitated processing for visual stimuli (Azevedo et al, 2018(Azevedo et al, , 2017Garfinkel et al, 2014;Pramme, Larra, Schächinger, & Frings, 2014, 2016 and increased oculomotor activity (Ohl et al, 2016) during early phases of the cardiac cycle, we here hypothesized that active information sampling (i.e., self-initiated action toward a visual stimulus) shows periodic variations with the phase of our heartbeat. To investigate perception and action within a comprehensive framework of mind-brain-body interactions, we studied cardiac-related sensorimotor processing in a self-paced visual sampling paradigm, in which participants decide when to press a key to see a task-relevant visual stimulus.…”