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Interoceptive processes emanating from baroreceptor signals support emotional functioning. Previous research suggests a unique link to fear: fearful faces, presented in synchrony with systolic baroreceptor firing draw more attention and are rated as more intense than those presented at diastole. This study examines whether this effect is unique to fearful faces or can be observed in other emotional faces. Participants (n = 71) completed an emotional visual search task (VST) in which fearful, happy, disgust and sad faces were presented during systolic and diastolic phases of the cardiac cycle. Visual search accuracy and emotion detection accuracy and latency were recorded, followed by a subjective intensity task. A series of interactions between emotion and cardiac phase were observed. Visual search accuracy for happy and disgust faces was greater at systole than diastole; the opposite was found for fearful faces. Fearful and happy faces were perceived as more intense at systole. Previous research proposed that cardiac signalling has specific effects on the attention and intensity ratings for fearful faces. Results from the present tasks suggest these effects are more generalised and raise the possibility that interoceptive signals amplify emotional superiority effects dependent on the task employed.
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More than meets the heart: Systolic amplification of different
emotional faces is task dependent
Leganes-Fonteneau, M.12*, Buckman, J.F.12, Suzuki, K.3, Pawlak, A.12, Bates,
M.E.12*
1Department of Kinesiology and Health, Rutgers University New Brunswick, NJ, USA
2 Cardiac Neuroscience Laboratory, Center of Alcohol Studies, Rutgers University New Brunswick, NJ,
USA
3Sackler Centre for Consciousness Science, University of Sussex - Brighton, Brighton and Hove, UK
*Corresponding authors:
Mateo Leganes-Fonteneau mateo.leganes@rutgers.edu - Phone: +1 848-445-2301 Fax: N/A
Marsha Bates mebates@smithers.rutgers.edu - Phone: +1 848-445-3559
Keywords: Emotion, Interoception, Visual Search Task, Face detection
The data that support the findings of this study are openly available in OSF at
http://DOI 10.17605/OSF.IO/S2EW9.
Abstract:
Interoceptive processes emanating from baroreceptor signals support emotional functioning. Previous
research suggests a unique link to fear: fearful faces, presented in synchrony with systolic baroreceptor
firing draw more attention and are rated as more intense than those presented at diastole. This study
examines whether this effect is unique to fearful faces or can be observed in other emotional faces.
Participants (n=71) completed an emotional visual search task (VST) in which fearful, happy, disgust and
sad faces were presented during systolic and diastolic phases of the cardiac cycle. Visual search accuracy
and emotion detection accuracy and latency were recorded, followed by a subjective intensity task.
A series of interactions between emotion and cardiac phase were observed. Visual search accuracy for
happy and disgust faces was greater at systole than diastole; the opposite was found for fearful faces.
Fearful and happy faces were perceived as more intense at systole.
Previous research proposed that cardiac signaling has specific effects on the attention and intensity
ratings for fearful faces. Results from the present tasks suggest these effects are more generalized and
raise the possibility that interoceptive signals amplify emotional superiority effects dependent on the
task employed.
Introduction:
Interoception is the integration of afferent physiological signals with higher order neural signals to
generate adaptive responses, particularly in emotional domains (Craig 2003; Critchley & Garfinkel 2017).
Memories for emotional words (Garfinkel et al. 2013), the mapping of physiology onto memory for
appetitive picture stimuli (Leganes‐Fonteneau et al. 2020), and the integration of subjective and neural
responses towards emotional picture stimuli (Pollatos et al. 2007) are all mediated via interoceptive
mechanisms.
There is strong evidence that cardiovascular mechanisms play a central role in interception. Cardiac
interoception is multidimensional, but specific attention has been paid to phasic cardiac signals
triggered by baroreceptors, which can affect emotional and cognitive processing (Critchley & Garfinkel
2017). Arterial baroreceptors are stretch sensitive mechanoreceptors triggered when each systolic
cardiac contraction pumps blood out of the heart. The baroreceptors relay information about the timing
and strength of each individual heartbeat to the brain, which uses it to coordinate sympathetic and
parasympathetic neural responses. Thus, baroreceptor firing provides a structured temporal framework
for deconstructing the role of phasic cardiac interoceptive signaling on cognitive and emotional
processing. Interoceptive studies use this framework to compare cognitive-emotional responses to
stimuli presented in synchrony with the R-wave (upward deflection of the QRS complex of the
electrocardiogram) which occurs at the end of the diastolic cardiac phase when baroreceptors are silent,
with stimuli presented 300ms after the R-wave, during the systolic phase and when baroreceptor firing
is estimated to be maximal (Gray et al. 2010).
The presentation of emotional stimuli in synchrony with baroreceptor firing has been examined using a
variety of tasks, and allows inferring the role of interoceptive signals in emotional processing. For
example, fearful faces presented during systole compared to diastole result in greater subjective ratings
of intensity (Garfinkel et al. 2014). More objective measures, such as an emotional attentional blink, also
show that fearful faces presented at systole are also more easily detected, as opposed to happy, disgust
and neutral faces (Garfinkel et al. 2014). Similar results were found using a spatial cueing task (Azevedo
et al. 2018); although in this case only responses for fearful and neural faces were compared. Taken
together, results from these studies highlight the role of cardiac signals in attentional engagement
towards salient stimuli and the automatic processing of cues. They also emphasize the role of
interoception on fear processing, and have been used to suggest that baroreceptor signaling selectively
increases the perception of fearful faces because of their relevance as a marker of threat (Garfinkel &
Critchley 2016), reflecting a distinct neural mechanism that underpins fear processing. This latter point is
supported by the fact that some experiments also investigated responses to disgust and happy faces
without finding a significant effect of cardiac phase (Garfinkel et al. 2014; Pfeifer et al. 2017), in line with
the hypothesis that different physiological signals support specific emotional processes (Friedman 2010).
The finding that interoceptive signals increase the perception of fearful faces parallels the so-called
threat advantage effect observed in multiple instances of emotional face research. This effect posits that
attentional responses towards aversive or threatening stimuli are higher than towards positive or
neutral stimuli (i.e. Öhman et al. 2001). However, threat advantage has proven to be highly task-
dependent (Lundqvist et al. 2014). In fact, superiority effects have been observed for happy rather than
fearful faces using emotional visual search tasks (i.e. Williams et al. 2005). Such visual search tasks are
unique in allowing insight into different factors underlying emotional face detection (Calvo &
Nummenmaa 2008) such as the perceptual salience and physical features of the faces. Moreover, a
visual search task, as opposed to other attentional paradigms, allows capturing attentional processes
more representative of the naturalistic scanning of faces in a crowd (Calvo & Nummenmaa 2008).
The evidence for the effects of baroreceptor signaling in fear processing is strong, but limited. Likewise,
definitive evidence of the specificity of cardiac interoception for fear processing is lacking and it seems
necessary to further investigate this topic using other paradigms. To test whether interoceptive signals
can amplify other emotional faces, we adapted a visual search task to study automatic attention
allocation towards emotional faces (fear, sad, happy and disgust) when stimuli were presented at
different phases of the cardiac cycle. Moreover, we administered an emotional intensity task (Garfinkel
et al. 2014) seeking to replicate previous results. We expected an interaction between cardiac cycle and
emotional cue on face detection and subjective intensity ratings. Based on previous literature, increased
responses at systole should be found for fearful faces. The emotional VST may also reveal effects for
happy faces, according to previous findings using this task, while the other emotional stimuli served as
exploratory controls.
Methods:
Participants:
A power analysis performed using results from Garfinkel et al. (2014), ηp²=0.33, revealed that a sample
of 45 participants would be sufficient to generate power = 0.95. Considering that these tasks were part
of a more extensive protocol, we decided to increase sample size by 50%.
A sample of 71 young adults (mean age=20.31, SD=2.74, 22 men) was recruited from undergraduate
students at the Rutgers University, New Jersey (USA). Participants were eligible if they had normal or
corrected-to-normal vision and reported not having any serious health issue, cardiac abnormalities, or
mental disorders in the past two years. Participants under pharmacological treatment (except birth
control) were excluded to avoid any interactions with the experiment. This study was approved by the
university Institutional Review Board for the Protection of Human Subjects Involved in Research.
Participants received compensation, either as $7/hour or course credits.
Tasks
Emotional Visual Search Task
This task assessed participants’ ability to detect emotional faces within a visual array (Williams et al.
2005). The visual array consisted of 6 faces organized in a circular pattern around the center of the
screen. Within a given trial, all faces belonged to the same actor, but one face expressed a full-blown
emotion (fear, sad, disgust or happy); the other 5 faces were emotionally neutral and served as
distractors. In total, participants completed 200 trials (50 per emotion) that used faces from 50 different
actors (28 females) extracted from the The Karolinska Directed Emotional Faces data base (Lundqvist et
al. 1998). All faces were presented in black and white and cropped around the facial oval, (Figure 1A).
Each trial started with the presentation of a red fixation point that remained on screen until the stimulus
array began. On 50% of the trials, the stimulus array appeared in synchrony with the participant’s R-
wave (diastolic trials). On the other 50% of trials, the array appeared 300ms after the R-wave to
approximate the systole (systolic trials). Trial presentation was fully randomized across emotion and
cardiac synchrony.
R-waves were detected using a Nonin 8000SM Finger Pulse Oximeter processed through a C# script that
then relayed information via UDP to Matlab for stimulus presentation. R-waves were predicted from the
mean of the 4 previous RRI intervals. The script accounted for 250ms for pulse transit time, including
25ms for delays in signal processing (Suzuki et al. 2013).
The stimulus array appeared for 100ms, followed by a black screen for 20ms. An objective response
array, which consisted of 6 white ovals at the location of the previously presented faces, then appeared.
Participants were asked to select the oval in which the emotional face had appeared as quickly and
accurately as possible using a computer mouse. Finally, participants saw a subjective response array,
consisting on 4 words in a row: Fear, Disgust, Sad, Happy. Participants were instructed to select the
emotional word that had been presented by using the mouse. Response arrays remained on screen until
a response was detected. The cursor location was reset to the center of the screen (fixation point) at the
end of each trial.
Pilot studies showed strong individual differences in objective emotional detection dependent on the
distance between the stimuli and the center of the screen. A too high visual search accuracy could
generate ceiling effects and blur the effect of cardiac phase. To control for these differences,
participants first completed a practice block, in which stimuli (the same ones used in the main task)
were not timed to cardiac signals, to calibrate accuracy in relation to the location of the faces. The
distance between stimuli and the center of the screen increased from 110px to 155px across 60 trials
using 15px intervals every 12 trials (3 trials per emotion). Accuracy scores were computed for each
interval and the largest interval at which accuracy was nearest to < 55% (chance level =1/6) was selected
for the main task. That average distance was 135px (SD<15).
Emotional Intensity task:
Participants were presented with one face at a time in the center of the screen for 150ms each. Faces
were synchronized with participants’ systole (50% trials) or diastole (50% trials). Participants were asked
to rate the intensity of each face using a visual analog scale, from “not at all intense(0) to “very
intense (100) (Figure 1B). Stimuli and trial schedule (i.e. number of stimuli per condition) were identical
to the Emotional VST.
Figure 1 A- Emotional Visual Search Task, B-Emotional Intensity Task: In the Emotional Visual Search
Task (A), participants saw a target emotional face on the screen (Fear, Happy, Sad or Disgust)
surrounded by 5 neutral distractors. In half of the trials, stimulus presentation was synchronized with
cardiac Diastolic phase and on the other half with the Systolic phase. Participants were asked to indicate
the location of the target emotional face (Objective response-Visual search accuracy) and indicate which
kind of emotion they saw on the screen (Subjective response-Emotion detection accuracy). In the
Emotional Intensity Task, participants were presented with a single emotional face at Systole or Diastole
and were asked to rate its intensity level on a visual analog scale.
Procedure
Participants were screened for eligibility using an online survey before completing one experimental
session in the laboratory. Upon arrival at the laboratory, participants provided written informed consent
and completed questionnaires (described in the Appendix section). Participants sat comfortably ~60cm
in front of a 19” computer screen. ECG sensors (Thought Technology Ltd, Montreal, Quebec) were
attached to participants and their physiological state was measured as part of the larger experimental
design during a 5-minute baseline task (usable data for 52 subjects, mean heart rate (HR) = 78.80).
Participants also completed two tasks measuring baseline individual differences in interoceptive
awareness (data not shown). Finally, participants performed the Emotional VST and Emotional Intensity
tasks, in that order.
Data extraction and analysis:
All data were extracted and averaged separately by emotion type and cardiac phase (systole vs.
diastole). Visual search accuracy was measured from the objective response array as the proportion of
correctly detected emotional face locations in the stimulus array. Emotion detection accuracy was
measured from the subjective response array as the proportion of correctly detected emotional
categories. Latencies for objective and subjective responses were computed as reaction times for
accurate responses (min single trial latency for objective =0.305ms (disgust face) and subjective=
0.202ms (fearful face) responses). For the Emotional Intensity task, intensity ratings were computed
from 0 to 100. Accuracy and intensity scores were transformed using arcsine square root.
A series of 2-way mixed model ANOVAs examined the interaction between emotion type and cardiac
timing on accuracies and latencies for visual search and emotion detection. An equivalent analysis was
performed on intensity ratings. Significant interactions were followed by post-hoc paired samples t-tests
assessing the effect of cardiac synchrony on each emotion.
An exploratory covariate analysis with questionnaire scores and cardiovascular indices is presented in
the Appendix.
Results:
Visual search accuracy:
We found a significant main effect of emotion type, F(3,490)=143.750, p<.001, ηp2=.47, and a significant
interaction between emotion type and cardiac synchrony, F(3,490)=11.880, p<.001, ηp2=.068, on visual
search accuracy scores. There was no significant main effect of cardiac synchrony, F(1,490)=1.270,
p=.261. Post-hoc paired samples t-tests compared accuracy scores between systole/diastole for each
emotion type. We found that visual search accuracy in systole trials was significantly higher than in
diastole trials for disgust, t(490)=-2.010, p=.0453, and happy faces, t(490)=-4.400, p<.001. Conversely,
we found that visual search accuracy in diastole trials was significantly higher than in systole trials for
fearful faces, t(490)=3.040, p=.0025. There was no significant effect of cardiac phase for sad faces,
t(490)=1.000, p=.319, see Figure 2A.
The analysis of differences in latencies by cardiac synchrony identified a main effect of synchrony, with
latencies being lower at diastole than systole, F(1, 490) = 14.00, p<.001, ηp2=.028; and emotion, F(3,
490) = 17.63, p<.001, ηp2=.097, but no significant interaction between emotion and synchrony,
F(3,490)=1.75, p=.156. See Table A1 in the Appendix for descriptive statistics.
Emotion detection Accuracy:
We found a significant main effect of emotion, F(3,490)=113.290, p<.001, ηp2=.41, and cardiac phase,
F(1,490)=10.990, p=.001, ηp2=.022, on emotion detection accuracy. There was also a significant
interaction between emotion and cardiac phase, F(3,490)=6.090, p<.001, ηp2=.036. Post-hoc paired
samples t-tests compared accuracy scores between systole/diastole for each emotion type. We found
that emotion detection accuracy in diastole trials was significantly higher than in systole trials for fear,
t(490)=3.670, p<.001, and sad, t(490)=2.790, p=.006, faces . There was no significant effect of cardiac
phase for disgust, t(490)=-1.280, p=.201, and happy, t(490)=0.840, p=.4, faces. See Figure 2B.
The analysis of differences in latencies found a main effect of emotion, F(3,490)=32.35, p<.001, ηp2=.17,
but no significant main effect of synchrony, F(1,490)=1.36, p=.245 or interaction between emotion and
synchrony, F(3,490)=2.01, p=.112. See Table A2 in Appendix for descriptive statistics.
Intensity Ratings:
We found a significant main effect of emotion, F(3,469)=102.000, p<.001, ηp2=.39, and cardiac phase,
F(1,469)=7.610, p=.006, ηp2=.016, on intensity ratings. There was also a significant interaction between
emotion and cardiac phase, F(3,469)=19.040, p<.001, ηp2=.039.
Post-hoc paired samples t-tests compared intensity between systole/diastole for each emotion type. We
found that intensity ratings in systole trials were significantly higher than in diastole trials for fear,
t(469)=3.720, p=.0002, and happy, t(469)=3.950, p<.001, faces. Conversely, we found that intensity
ratings in diastole trials were significantly higher than in systole trials for disgust faces, t(469)=3.770,
p=.0002. There was no significant effect of cardiac phase for sad faces, t(469)=01.010, p=.314. See Figure
2C.
Figure 2 A Visual Search accuracy, B Emotion Detection accuracy, C Intensity ratings: Task scores
as a function of emotion and cardiac synchrony. Accuracy scores were computed as the mean
proportion of correct responses. Error bars represent SE.
Discussion:
The purpose of this study was to expand previous research on the role of cardiac signals in the detection
of emotional faces. By adapting an Emo-VST to present emotional faces in synchrony with baroreceptor
signals, we attempted to provide new insight into the interoceptive correlates of emotion. We included
four emotional face sets (happy, fear, sad, disgust) and found that cardiac interoceptive signals
contributed to cognitive-emotional processing beyond fear. The results did not uniformly support our
hypotheses, but rather suggest that afferent baroreceptor signaling supports emotional processing
depending on the experimental paradigm employed.
Specifically, participants showed poorer visual search and emotion detection accuracy for fearful faces,
but greater intensity ratings when stimuli were presented at systole versus diastole. While the intensity
finding replicates Garfinkel el al. (2014), the poorer accuracy does not support the role of interoceptive
signals exclusively for fearful faces. This could be due to the fact that previous experimental paradigms
were based on tasks for which aversive stimuli show a superiority effect. For example, the emotional
attentional blink task used by Garfinkel et al. (2014) has repeatedly been shown to capture enhanced
interference by aversive stimuli (Leganes-Fonteneau et al. 2018). Similarly, spatial cueing tasks, such as
the one used by Azevedo and colleagues (2018) are more sensitive to threatening stimuli (Cisler &
Olatunji 2010).
The Emotional VST on the other hand typically elicits superiority effects for happy faces and an inhibition
of fearful faces (Williams et al. 2005). This is consistent with our findings that participants showed
greater visual search accuracy for happy faces when stimuli were presented at systole versus diastole.
Accuracy for emotion detection of happy faces did not differ as ceiling effects may have blurred the
effect of systolic amplification. Finding that happy faces also are perceived as more intense at systole
extends previous results obtained by Garfinkel el al. (2014), confirming that interoceptive signals do not
exclusively amplify the subjective perception of fearful faces. We also found an increase in visual search
accuracy for disgust faces presented at systole, although the effect was lesser than for happy faces, in
line again with previous results in an emotional VST showing higher responsiveness for happy and
disgust faces over fearful ones (Calvo & Nummenmaa 2008).
The inhibition at systole of visual search and emotion detection accuracy for fearful faces we observed
can be interpreted according to Williams et al. (2005), who proposed that fearful faces were less
detectable on a VST because they would signal imminent threat, directing subjects’ attention towards
the surrounding faces. That same rationale could be applied to our results, and systolic presentation of
fearful faces could have increased their ability to signal threat, directing attention towards the other
faces in the stimulus array more effectively and decreasing visual search and emotion detection
accuracy. The discussion of the attentional mechanisms supporting superiority effects for one or
another emotion are beyond the scope of this brief report, but they could be attributed to the
perceptual characteristics of the different faces and their salience (Calvo & Nummenmaa 2008;
Lundqvist et al. 2015). In this experiment, beyond prior observations with fear faces and the expected
superiority effects of happy faces, we observed the effect of cardiac signaling on disgust faces (greater
visual search accuracy at systole) and sad faces (poorer accuracy of emotion detection at systole).
Importantly, the flexibility of the emotional VST to incorporate different combinations of stimuli as
targets or distractors, different instructions, or experimental techniques (i.e. eye tracking) can play a
useful role in clarifying the interaction between emotional processing and cardiac signaling.
Importantly, we were not able to characterize the reliability of the R-wave prediction, but replication of
previous findings (Garfinkel et al. 2014) supports the methodology we used. Future studies should
include replication using more advanced and precise cardiac timing procedures.
Conclusions
Interoceptive deficits are proposed as a source of emotional impairment in a variety of psychiatric
disorders (i.e. anxiety, autism spectrum disorders, depression; reviewed in Khalsa et al., (2017)).
Individuals with the most prevalent psychiatric disorders often exhibit critical deficits in processing
happy and sad stimuli (Joormann & Gotlib 2007), yet the few existing studies have suggested specificity
of cardiac interoceptive signaling for fearful stimuli.
This study suggests that the specificity of interoception for fearful stimuli may be a task-based artifact,
as other emotions (happy, disgust) were amplified by cardiac signals. Although this goes against current
perspectives on the autonomic specificity of emotion (Friedman 2010), our results are consistent with
cardiac outputs as an undifferentiated interoceptive signal of general arousal feeding into evaluative
cognitive operations (Cacioppo et al. 2000). Clearly, more research is needed, but it is possible that our
novel emotional VST task may allow a broader assessment of the interoceptive correlates of emotional
processing in clinical populations. Future research aimed directly at disentangling the relationship
between interoceptive signals and the cognitive and attentional factors driving emotional processing
(Galvez-Pol et al. 2020) is needed.
Furthermore, based on evidence that baroreceptor signaling can be modulated through resonance
paced breathing to possibly increase interoceptive awareness (Leganes-Fonteneau et al. In press), the
emotional VST could be used to examine whether resonance breathing can tighten the link between
interoceptive signals and emotional face detection as a prospective clinical tool.
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... By time-locking the presentation of a brief single stimulus to the systolic period (i.e., ~200-400 ms after the electrocardiogram's [ECG's] R-peak, when the baroreceptors are maximally represented in brain) or to the diastolic period (i.e., the remainder of the cardiac cycle, which corresponds to a period of baroreceptor quiescence), recent studies have documented the influence of these cardiac afferent signals (i.e., at systole vs. diastole) in several sensory and cognitive domains (Ambrosini et al., 2019;Azzalini et al., 2019;. Most notably, afferent cardiac signals contribute to an upregulation of motivationally salient stimuli, such as fearful faces, which are more easily detected (Garfinkel et al., 2014;but see Leganes-Fonteneau et al., 2021), engage more attentional resources (Azevedo et al., 2018), and are judged as more intense (Garfinkel et al., 2014;Leganes-Fonteneau et al., 2021) when perceived during systole than during diastole. It is argued that such enhancement in the processing of threat signals reflects a selective influence of physiology on motivational systems to direct resources toward relevant impending information . ...
... Again, only the main effect of rhythm, and not its interaction with trustworthiness levels, was found to be significant (see the Supplemental Material), confirming that the observed effects did not seem to depend on morphological features typically associated with trustworthiness or untrustworthiness. This pattern provides a conceptual replication of Study 1 by showing that faces presented in synchrony with participants' hearts are judged as less trustworthy, consistent with the cardiac cycle literature showing increased sensitivity to threat-related stimuli (Azevedo et al., 2018;Garfinkel & Critchley, 2016;Garfinkel et al., 2014Garfinkel et al., , 2021Leganes-Fonteneau et al., 2021) and diminished trustworthiness ratings (Li et al., 2020) when faces are presented during cardiac systole. However, both Studies 1 and 2 implemented the cardiovisual synchrony manipulation only during systolic periods. ...
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When we see new people, we rapidly form first impressions. Whereas past research has focused on the role of morphological or emotional cues, we asked whether transient visceral states bias the impressions we form. Across three studies ( N = 94 university students), we investigated how fluctuations of bodily states, driven by the interoceptive impact of cardiac signals, influence the perceived trustworthiness of faces. Participants less often chose faces presented in synchrony with their own cardiac systole as more trustworthy than faces presented out of synchrony. Participants also explicitly judged faces presented in synchrony with their cardiac systole as less trustworthy. Finally, the presentation of faces in synchrony with participants’ cardiac diastole did not modulate participants’ perceptions of the faces’ trustworthiness, suggesting that the systolic phase is necessary for such interoceptive effects. These findings highlight the role of phasic interoceptive information in the processing of social information and provide a mechanistic account of the role of visceroception for social perception.
... However, this analysis does not consider the biphasic nature of the cardiac cycle (systole and diastole phases). Yet, previous studies have shown that responses to stimuli vary as a function of the phase of the cardiac cycle in which information is processed (see e.g., Garfinkel et al., 2014;Al et al., 2020;Leganes-Fonteneau et al., 2020;Grund et al., 2022). Therefore, we also examined participants' responses as a function of the phase of the cardiac cycle. ...
... The previous analysis considers the repeating nature of the cardiac cycle, but it does not consider its biphasic nature. Previous studies have shown that responses to stimuli vary as a function of the phase of the cardiac cycle in which information is processed (i.e., systole and diastole; e.g., Garfinkel et al., 2014;Al et al., 2020;Leganes-Fonteneau et al., 2020;Grund et al., 2022). In a second analysis, we examined participants' responses as a function of the phase of the cardiac cycle, systole or diastole. ...
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Perception and cognition are modulated by the phase of the cardiac signal in which the stimuli are presented. This has been shown by locking the presentation of stimuli to distinct cardiac phases. However, in everyday life sensory information is not presented in this passive and phase-locked manner, instead we actively move and control our sensors to perceive the world. Whether active sensing is coupled and modulated with the cardiac cycle remains largely unknown. Here we recorded the electrocardiograms of human participants while they actively performed a tactile grating orientation task. We show that the duration of subjects’ touch varied as a function of the cardiac phase in which they initiated it. Touches initiated in the systole phase were held for longer periods of time than touches initiated in the diastole phase. This effect was most pronounced when elongating the duration of the touches to sense the most difficult gratings. Conversely, while touches in the control condition were coupled to the cardiac cycle, their length did not vary as a function of the phase in which these were initiated. Our results reveal that we actively spend more time sensing during systole periods, the cardiac phase associated with lower perceptual sensitivity (vs. diastole). In line with interoceptive inference accounts, these results indicate that we actively adjust the acquisition of sense data to our internal bodily cycles.
... Similarly, other studies have shown an enhancement of attentional capture for threatrelated stimuli presented during cardiac systole in the attentional engagement task (Azevedo et al., 2018). In addition, recent studies have reported that processing positively valenced stimuli (i.e., monetary rewards and happy faces) can be facilitated during cardiac systole (Kimura, 2019;Leganes-Fonteneau et al., 2021). Therefore, previous results have suggested that the natural fluctuation of cardiac afferent signals causes moment-tomoment fluctuations in the processing of stimuli associated with motivational/affective significance. ...
... Since previous studies have demonstrated that the effect of the cardiac cycle on affective processing could depend on stimulus valence (e.g., Garfinkel et al., 2014;Azevedo et al., 2018;Kimura, 2019;Leganes-Fonteneau et al., 2021), we used a modified version of the Q-learning model in which learning from positive and negative prediction errors is determined by different learning rates, according to previous studies (e.g., Lefebvre et al., 2017). The modified version of the Q-learning model, referred to as the Q-A model, allows the learning rates to differ depending on the sign of the prediction error, as follows: ...
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This study aimed to investigate whether instrumental reward learning is affected by the cardiac cycle. To this end, we examined the effects of the cardiac cycle (systole or diastole) on the computational processes underlying the participants’ choices in the instrumental learning task. In the instrumental learning task, participants were required to select one of two discriminative stimuli (neutral visual stimuli) and immediately receive reward/punishment feedback depending on the probability assigned to the chosen stimuli. To manipulate the cardiac cycle, the presentation of discriminative stimuli was timed to coincide with either cardiac systole or diastole. We fitted the participants’ choices in the task with reinforcement learning (RL) models and estimated parameters involving instrumental learning (i.e., learning rate and inverse temperature) separately in the systole and diastole trials. Model-based analysis revealed that the learning rate for positive prediction errors was higher than that for negative prediction errors in the systole trials; however, learning rates did not differ between positive and negative prediction errors in the diastole trials. These results demonstrate that the natural fluctuation of cardiac afferent signals can affect asymmetric value updating in instrumental reward learning.
... Put simply, precise visual information is only available during certain parts of the cardiac cycle, which itself depends upon the state of arousal (i.e., the policy currently inferred and selected). This can be thought of as a simple approximation of cardiac and other bodily timing effects, expressed as a momentary occlusion or attenuation of sensory input by (for example) afferent inhibitory baroreceptor effects [3,7,8,12,17,32,[61][62][63], or by the Fig 2. The generative model. This schematic illustrates how hidden states cause each other and sensory outcomes in the interoceptive and exteroceptive domain. ...
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A growing body of evidence highlights the intricate linkage of exteroceptive perception to the rhythmic activity of the visceral body. In parallel, interoceptive inference theories of affective perception and self-consciousness are on the rise in cognitive science. However, thus far no formal theory has emerged to integrate these twin domains; instead, most extant work is conceptual in nature. Here, we introduce a formal model of cardiac active inference, which explains how ascending cardiac signals entrain exteroceptive sensory perception and uncertainty. Through simulated psychophysics, we reproduce the defensive startle reflex and commonly reported effects linking the cardiac cycle to affective behaviour. We further show that simulated 'interoceptive lesions' blunt affective expectations, induce psychosomatic hallucinations, and exacerbate biases in perceptual uncertainty. Through synthetic heart-rate variability analyses, we illustrate how the balance of arousal-priors and visceral prediction errors produces idiosyncratic patterns of physiological reactivity. Our model thus offers a roadmap for computationally phenotyping disordered brain-body interaction.
... Put simply, precise visual information is only available during certain parts of the cardiac cycle, which itself depends upon the state of arousal (i.e., the policy currently inferred and selected). This can be thought of as a simple approximation of cardiac and other bodily timing effects, expressed as a momentary occlusion or attenuation of sensory input by (for example) afferent inhibitory baroreceptor effects [3,7,8,12,17,32,[61][62][63], or by the Fig 2. The generative model. This schematic illustrates how hidden states cause each other and sensory outcomes in the interoceptive and exteroceptive domain. ...
Article
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A growing body of evidence highlights the intricate linkage of exteroceptive perception to the rhythmic activity of the visceral body. In parallel, interoceptive inference theories of affective perception and self-consciousness are on the rise in cognitive science. However, thus far no formal theory has emerged to integrate these twin domains; instead, most extant work is conceptual in nature. Here, we introduce a formal model of cardiac active inference, which explains how ascending cardiac signals entrain exteroceptive sensory perception and uncertainty. Through simulated psychophysics, we reproduce the defensive startle reflex and commonly reported effects linking the cardiac cycle to affective behaviour. We further show that simulated ‘interoceptive lesions’ blunt affective expectations, induce psychosomatic hallucinations, and exacerbate biases in perceptual uncertainty. Through synthetic heart-rate variability analyses, we illustrate how the balance of arousal-priors and visceral prediction errors produces idiosyncratic patterns of physiological reactivity. Our model thus offers a roadmap for computationally phenotyping disordered brain-body interaction.
... However, contrary results have been reported for visual selection, where the selection efficiency of target among distractors and attentional inhibition of masking stimuli appear enhanced at systole compared to diastole (Pramme et al., 2016;. The evidence around emotional perception is also mixed -while Garfinkel and colleagues (2014) found that both detection and rated intensity of fearful face images were enhanced at systole, a later study by Leganes-Fonteneau et al.(2020) also showed increased rated intensity but a reduction in visual search accuracy for fearful faces (although an increased accuracy for happy and disgust expressions). Nonetheless, it has been noted that affective value of the stimuli may modulate their relationship with cardiac phase (Allen, Levy, Parr, & Friston, 2019). ...
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SKORA, L.I., J.J.A. LIVERMORE and K. Roelofs. The functional role of cardiac activity in perception and action. NEUROSCI BIOBEHAV REV X(X) XXX-XXX, 2022. Patterns of cardiac activity continuously vary with environmental demands, accelerating or decelerating depending on circumstances. Simultaneously, cardiac cycle affects a host of higher-order processes, where systolic baroreceptor activation largely impairs processing. However, a unified functional perspective on the role of cardiac signal in perception and action has been lacking. Here, we combine the existing strands of literature and use threat-, anticipation-, and error-related cardiac deceleration to show that deceleration is an adaptive mechanism dynamically attenuating the baroreceptor signal associated with each heartbeat to minimise its impact on exteroceptive processing. This mechanism allows to enhance attention afforded to external signal and prepare an appropriate course of action. Conversely, acceleration is associated with a reduced need to attend externally, enhanced action tendencies and behavioural readjustment. This novel account demonstrates that dynamic adjustments in heart rate serve the purpose of regulating the level of precision afforded to internal versus external evidence in order to optimise perception and action. This highlights that the importance of cardiac signal in adaptive behaviour lies in its dynamic regulation.
... In contrast with past conceptualizations, these factors include both conscious and non-conscious interoceptive processes, which is consistent with the definition of interoception we have proposed. Non-conscious interoceptive processes might, for instance, be measured through neuroimaging techniques, which track brain activations related to interoception, or indirect measures, which evaluate the impact of internal signals on motor reflexes (e.g., startle reflex; Alius et al., 2015), visual processing (e.g., Leganes-Fonteneau et al., 2021), and cognitive functions (Garfinkel et al., 2020). ...
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Interoception has been the object of renewed interest over the past two decades. The involvement of interoception in a diverse range of fundamental human abilities (e.g., decision-making and emotional regulation) has led to the hypothesis that interoception is a central transdiagnostic process causing and maintaining mental disorders as well as physical diseases. However, interoception has been inconsistently defined and conceptualized. In the first part of this article, we argue that the widespread practice of defining interoception as the processing of signals originating from within the body and limiting it to specific physiological pathways (lamina I spinothalamic afferents) is problematic. This is because the processing of internal states is underpinned by other physiological pathways, generally assigned to the somatosensory system. In the second part, we explain that the consensual dimensions of interoception are empirically detached from existing measures, the latter of which capture loosely-related phenomena. This is detrimental to the replicability of findings across measures and the validity of interpretations. In the general discussion, we discuss the main insights of the current analysis and suggest a more refined way to define interoception and conceptualize its underlying dimensions.
... People refer to inner bodily sensations when describing their intentions, emotions, and mental experiences. Increasingly research supports the influence of afferent signalling, such as heartbeats, upon cognition, movement, and perception (e.g., Galvez-Pol et al., 2022Galvez-Pol et al., 2020bGarfinkel et al., 2020;Leganes-Fonteneau et al., 2020). Although of considerable interest, these demonstrations usually adopt a rather individualistic perspective: physiological bodily signals serve 'one's purpose'. ...
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For more than a century it has been proposed that visceral and vasomotor changes inside the body influence and reflect our experience of the world. For instance, cardiac rhythms (heartbeats and consequent heart rate) reflect psychophysiological processes that underlie our cognition and affective experience. Yet, considering that we usually infer what others do and feel through vision, whether people can identify the most likely owner of a given bodily rhythm by looking at someone’s face remains unknown. To address this, we developed a novel two-alternative forced-choice task in which 120 participants watched videos showing two people side by side and visual feedback from one of the individuals’ heartbeats in the centre. Participants’ task was to select the owner of the depicted heartbeats. Across five experiments, one replication, and supplementary analyses, the results show that: i) humans can judge the most likely owner of a given sequence of heartbeats significantly above chance levels, ii) that performance in such a task decreases when the visual properties of the faces are altered (inverted, masked, static), and iii) that the difference between the heart rates of the individuals portrayed in our 2AFC task seems to contribute to participants’ responses. While we did not disambiguate the type of information used by the participants (e.g., knowledge about appearance and health, visual cues from heartbeats), the current work represents the first step to investigate the possible ability to infer or perceive others’ cardiac rhythms. Overall, our novel observations and easily adaptable paradigm may generate hypotheses worth examining in the study of human and social cognition.
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This study investigates whether decision-making under uncertainty is influenced by the cardiac cycle. To test this hypothesis, we examined the influence of the cardiac cycle on an individual's decision-making process in a gambling experiment. Participants were asked to choose one option with a sure payout or uncertain option with varying degrees of winning probability, ambiguity, and monetary amounts. The onset of presentation of the options is timed to coincide with either cardiac ventricular systole or diastole. The results show that, for most participants, the risk aversion score was lower in the systole trial than in the diastole trial. Model-based exploratory analysis revealed that the higher propensity to take risks in the systole trial compared with that in the diastole trial could be captured better by the change in the gambling bias against the utility of the risky options, rather than by a change in risk attitude. The results provide evidence that the natural fluctuation of cardiac afferent signals can affect risky decision-making.
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Recent research has demonstrated that perception and reasoning vary according to the phase of internal bodily signals such as heartbeat. This has been shown by locking the presentation of sensory events to distinct phases of the cardiac cycle. However, task-relevant information is not usually encountered in such a phase-locked manner nor passively accessed, but rather actively sampled at one's own pace. Moreover, if the phase of the cardiac cycle is an important modulator of perception and cognition, as previously proposed, then the way in which we actively sample the world should be similarly modulated by the phase of the cardiac cycle. Here we tested this by coregistration of eye movements and heartbeat signals while participants freely compared differences between two visual arrays. Across three different analyses, we found a significant coupling of saccades, subsequent fixations, and blinks with the cardiac cycle. More eye movements were generated during the systolic phase of the cardiac cycle, which has been reported as the period of maximal effect of the baroreceptors' activity upon cognition. Conversely, more fixations were found during the diastole phase (quiescent baroreceptors). Lastly, more blinks were generated in the later period of the cardiac cycle. These results suggest that interoceptive and exteroceptive processing do adjust to each other; in our case, by sampling the outer environment during quiescent periods of the inner organism.
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Influential theories suggest emotional feeling states arise from physiological changes from within the body. Interoception describes the afferent signalling, central processing, and neural and mental representation of internal bodily signals. Recent progress is made in conceptualizing interoception and its neural underpinnings. These developments are supported by empirical data concerning interoceptive mechanisms and their contribution to emotion. Fresh insights include description of short-term interoceptive effects on neural and mental processes(including fear-specific cardiac effects), the recognition of dissociable psychological dimensions of interoception, and models of interoceptive predictive coding that explain emotions and selfhood (reinforced by structural anatomical models and brain and experimental findings). This growing grasp of interoception is enriching our understanding of emotion and its disorders.
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