Multisensory integration of anticipated cardiac signals with visual targets affects their detection among multiple visual stimuli.

Many studies have elucidated the multisensory processing of different exteroceptive signals (e.g., auditory-visual stimuli), but less is known about the multisensory integration of interoceptive signals with exteroceptive information. Here, we investigated the perceptual outcomes and electrophysiological brain mechanisms of cardio-visual integration by using participants' electrocardiogram signals to control the color change of a visual target in dynamically changing displays. Reaction times increased when the target change coincided with strong cardiac signals concerning the state of cardiovascular arousal (i.e., presented at the end of ventricular systole), compared to when the target change occurred at a time when cardiac arousal was relatively low (i.e., presented at the end of ventricular diastole). Moreover, the concurrence of the target change and cardiac arousal signals modulated the event-related potentials and the beta power in an early period (~100 ms after stimulus onset), and decreased the N2pc and the beta lateralization in a later period (~200 ms after stimulus onset). Our results suggest that the multisensory integration of anticipated cardiac signals with a visual target negatively affects its detection among multiple visual stimuli, potentially by suppressing sensory processing and reducing attention toward the visual target. This finding highlights the role of cardiac information in visual processing and furthers our understanding of the brain dynamics underlying multisensory perception involving both interoception and exteroception.

Response inhibition is disrupted by interoceptive processing at cardiac systole.

The present study investigated how cardiac signals influence response inhibition at both behavioral and electrophysiological levels by using participants' electrocardiogram signals to control the occurrence of events in a stop-signal task, in which the go cue was unpredictably followed by a stop signal requiring the cancellation of the prepotent response. We observed prolonged stop-signal reaction times, reduced stop-signal P3 amplitudes, and higher heartbeat evoked potential amplitudes when the stop signal was presented at cardiac systole, compared to presentation randomly within the cardiac cycle. These effects were independent of the emotional attribute of the stop signal (i.e., emotional facial expression change or non-emotional color change). Our results suggest that coupling stop signals to peripheral autonomic cardiac signals has an impeding effect on response inhibition, probably via shifting attention from exteroception to interoception. Our findings help clarify the precise impact of interoceptive signals on inhibitory control.

From the inside out: Interoceptive feedback facilitates the integration of visceral signals for efficient sensory processing.

Neuroscientific studies have mainly focused on the way humans perceive and interact with the external world. Recent work in the interoceptive domain indicates that the brain predictively models information from inside the body such as the heartbeat and that the efficiency with which this is executed can have implications for exteroceptive processing. However, to date direct evidence underpinning these hypotheses is lacking. Here, we show how the brain predictively refines neural resources to process afferent cardiac feedback and uses these interoceptive cues to enable more efficient processing of external sensory information. Participants completed a repetition-suppression paradigm consisting of a neutral repeating face. During the first face presentation, they heard auditory feedback of their heartbeat which either coincided with the systole of the cardiac cycle, the time at which cardiac events are registered by the brain or the diastole during which the brain receives no internal cardiac feedback. We used electroencephalography to measure the heartbeat evoked potential (HEP) as well as auditory (AEP) and visual evoked potentials (VEP). Exteroceptive cardiac feedback which coincided with the systole produced significantly higher HEP amplitudes relative to feedback timed to the diastole. Elevation of the HEP in this condition was followed by significant suppression of the VEP in response to the repeated neutral face and a stepwise decrease of AEP amplitude to repeated heartbeat feedback. Our results hereby show that exteroceptive heartbeat feedback coinciding with interoceptive signals at systole enhanced interoceptive cardiac processing. Furthermore, the same cue facilitating interoceptive integration enabled efficient suppression of a visual stimulus, as well as repetition suppression of the AEP across successive auditory heartbeat feedback. Our findings provide evidence that the alignment of external to internal signals can enhance the efficiency of interoceptive processing and that cues facilitating this process in either domain have beneficial effects for internal as well as external sensory processing.

Interoceptive cardiac expectations to emotional stimuli predict visual perception.

Previous work exploring the interplay between the processing of internal bodily signals and the perception of external events suggests a correlative relationship between both domains. Here, we demonstrate an experimentally induced link between visual perception and the emotional modulation of interoceptive cardiac signals. We pair an emotion repetition-suppression paradigm shown to modulate neural responses to heartbeats with a previously reported visual detection task. Using electrophysiological and cardiac measurements, we show that, relative to alternating facial expressions of emotions, repeating facial expressions evoke stable patterns of cardiac responses and that this iteration of the cardiac response leads to a distinct modulation of the heartbeat evoked potential (HEP) amplitude. Crucially, we were able to modulate the direction of the amplitude change to increase HEP expression in response to repeated emotionally neutral faces and decrease it by repeating angry faces. Visual detection accuracy was significantly higher in repeating, relative to alternating face trials. Furthermore, reduced HEP amplitude to repeated angry faces acted as a direct predictor of subsequently elevated detection performance. Our findings demonstrate that accurate top-down anticipation of the heartbeat signal coincides with enhanced exteroceptive visual perception, particularly in the context of emotional events. Findings hereby highlight the integrated nature of internal and external stimulus processing and implicate predictive interoceptive processes induced by emotions for the conscious perception of sensory input activated from outside of the body. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

I feel what I do: Relating interoceptive processes and reward-related behavior.

Interoceptive signalling has been shown to contribute to action regulation and action experience. Here, we assess whether motor behaviour can be influenced by anticipated homeostatic feeling states induced through different predictable contexts. Participants performed a reward incentive paradigm in which accurate responses increased (gain) or avoided the depletion (averted loss) of a credit score. Across two types of blocks, we varied the predictability of the outcome state. In predictable blocks, a cue signaled a gain, loss or control trial (motor response did not affect the credit score). This allowed participants to anticipate the interoceptive feeling state associated with the outcome. In unpredictable blocks, the cue had no relation to the type of outcome. Thus, participants were unable to anticipate the feeling state it produced. Via EEG, we measured the Heartbeat Evoked Potential (HEP) and the Contingent Negative Variation (CNV) as indices of interoceptive and motor processing respectively. In addition, we measured feedback P3 amplitude following outcome presentation and accuracy and reaction times of the required motor response. We observed higher HEP and CNV amplitudes as well as faster and more accurate motor responses in predictable compared to unpredictable outcome blocks. Similarly, feedback-related P3 amplitudes were significantly lower for predictable relative to unpredictable outcomes. Crucially, HEP amplitudes measured prior to feedback predicted feedback-related P3 amplitudes for anticipated outcome events. Results suggest that accurate anticipation of homeostatic feeling states associated with gain, loss or control outcomes facilitates motor execution and outcome evaluation. Findings are hereby the first to empirically assess the link between interoceptive and motor domains and provide primary evidence for a joint processing structure.

Affective interoceptive inference: Evidence from heart-beat evoked brain potentials.

The perception of internal bodily signals (interoception) is central to many theories of emotion and embodied cognition. According to recent theoretical views, the sensory processing of visceral signals such as one's own heartbeat is determined by top-down predictions about the expected interoceptive state of the body (interoceptive inference). In this EEG study we examined neural responses to heartbeats following expected and unexpected emotional stimuli. We used a modified stimulus repetition task in which pairs of facial expressions were presented with repeating or alternating emotional content, and we manipulated the emotional valence and the likelihood of stimulus repetition. We found that affective predictions of external socially relevant information modulated the heartbeat-evoked potential, a marker of cardiac interoception. Crucially, the HEP changes highly relied on the expected emotional content of the facial expression. Thus, expected negative faces led to a decreased HEP amplitude, whereas such an effect was not observed after an expected neutral face. These results suggest that valence-specific affective predictions, and their uniquely associated predicted bodily sensory state, can reduce or amplify cardiac interoceptive responses. In addition, the affective repetition effects were dependent on repetition probability, highlighting the influence of top-down exteroceptive predictions on interoception. Our results are in line with recent models of interoception supporting the idea that predicted bodily states influence sensory processing of salient external information.

Cardiac interoceptive learning is modulated by emotional valence perceived from facial expressions.

Interoception refers to the processing of homeostatic bodily signals. Research demonstrates that interoceptive markers can be modulated via exteroceptive stimuli and suggests that the emotional content of this information may produce distinct interoceptive outcomes. Here, we explored the impact of differently valenced exteroceptive information on the processing of interoceptive signals. Participants completed a repetition-suppression paradigm viewing repeating or alternating faces. In experiment 1, faces wore either angry or pained expressions to explore the interoceptive response to different types of negative stimuli in the observer. In experiment 2, expressions were happy or sad to compare interoceptive processing of positive and negative information. We measured the heartbeat evoked potential (HEP) and visual evoked potentials (VEPs) as a respective marker of intero- and exteroceptive processing. We observed increased HEP amplitude to repeated sad and pained faces coupled with reduced HEP and VEP amplitude to repeated angry faces. No effects were observed for positive faces. However, we found a significant correlation between suppression of the HEP and VEP to repeating angry faces. Results highlight an effect of emotional expression on interoception and suggest an attentional trade-off between internal and external processing domains as a potential account of this phenomenon.

Stress-related deficits of older adults' spatial working memory: an EEG investigation of occipital alpha and frontal-midline theta activities.

Studies highlight cumulative life stress as a significant predictor of accelerated cognitive aging. This study paired electrophysiological with behavioral measures to explore how cumulative stress affects attentional and maintenance processes underpinning working memory retention. We collected electroencephalographic recordings from 60 individuals (30 older, 30 younger) reporting high or low levels of cumulative stress during the performance of a spatial Sternberg task. We measured mid-occipital alpha (8-12 Hz) and frontal-midline theta (4-6 Hz) as indicators of attentional and maintenance processes. Older, high-stress participants' behavioral performance lay significantly below than that of younger adults and low-stress older individuals. Impaired task performance coincided with reduced event-related synchronization in alpha and theta frequency ranges during memory maintenance. Electrophysiological findings suggest that older adults' reduced performance results from a stress-related impact on their ability to retain a stimulus in working memory and inhibit extraneous information from interfering with maintenance. Our results demonstrate the wide-ranging impact of cumulative stress on cognitive health and provide insight into the functional mechanisms disrupted by its influence.

The Interaction between Interoceptive and Action States within a Framework of Predictive Coding.

The notion of predictive coding assumes that perception is an iterative process between prior knowledge and sensory feedback. To date, this perspective has been primarily applied to exteroceptive perception as well as action and its associated phenomenological experiences such as agency. More recently, this predictive, inferential framework has been theoretically extended to interoception. This idea postulates that subjective feeling states are generated by top-down inferences made about internal and external causes of interoceptive afferents. While the processing of motor signals for action control and the emergence of selfhood have been studied extensively, the contributions of interoceptive input and especially the potential interaction of motor and interoceptive signals remain largely unaddressed. Here, we argue for a specific functional relation between motor and interoceptive awareness. Specifically, we implicate interoceptive predictions in the generation of subjective motor-related feeling states. Furthermore, we propose a distinction between reflexive and pre-reflexive modes of agentic action control and suggest that interoceptive input may affect each differently. Finally, we advocate the necessity of continuous interoceptive input for conscious forms of agentic action control. We conclude by discussing further research contributions that would allow for a fuller understanding of the interaction between agency and interoceptive awareness.

Exteroceptive expectations modulate interoceptive processing: repetition-suppression effects for visual and heartbeat evoked potentials.

Interoception refers to the signaling of internal bodily commands. Here, we explore repetition suppression of intero- and exteroceptive neural markers to test whether the perception and predictability of exteroceptive stimulus material affects their expression. Participants completed a repetition suppression paradigm in which angry or neutral facial expressions repeated or alternated. Participants received either an implicit (experiment 1) or explicit (experiment 2) cue enabling the formation of expectations regarding the upcoming facial expression. We measured the heartbeat-evoked potential (HEP) indexing cardiac processing and visual evoked potentials (VEP) in response to viewing the second (repeated or alternated) face. Repeating angry facial expressions produced repetition suppression of both HEP and VEP amplitude while repeating neutral expressions led to repetition enhancement of HEP amplitude. This effect was magnified when participants were explicitly aware of predictive cues. Furthermore, repetition suppression of HEP amplitude correlated with neural attenuation of VEP activity. Results highlight repetition effects for interoceptive as well as exteroceptive neural markers and support top-down, expectation-based accounts of the phenomenon. Furthermore, results demonstrate that the perception of exteroceptive stimulus information has an effect on the processing of interoceptive signals and suggest a direct neural connection between the processing of external and internal sensory information.

The association between high levels of cumulative life stress and aberrant resting state EEG dynamics in old age.

Cumulative experienced stress produces shortcomings in old adults' cognitive performance. These are reflected in electrophysiological changes tied to task execution. This study explored whether stress-related aberrations in older adults' electroencephalographic (EEG) activity were also apparent in the system at rest. To this effect, the amount of stressful life events experienced by 60 young and 60 elderly participants were assessed in conjunction with resting state power changes in the delta, theta, alpha, and beta frequencies during a resting EEG recording. Findings revealed elevated levels of delta power among elderly individuals reporting high levels of cumulative life stress. These differed significantly from young high and low stress individuals and old adults with low levels of stress. Increases of delta activity have been linked to the emergence of conditions such as Alzheimer's Disease and Mild Cognitive Impairment. Thus, a potential interpretation of our findings associates large amounts of cumulative stress with an increased risk of developing age-related cognitive pathologies in later life.

Experienced stress produces inhibitory deficits in old adults' Flanker task performance: First evidence for lifetime stress effects beyond memory.

Studies regarding aged individuals' performance on the Flanker task differ with respect to reporting impaired or intact executive control. Past work has explained this discrepancy by hypothesising that elderly individuals use increased top-down control mechanisms advantageous to Flanker performance. This study investigated this mechanism, focussing on cumulative experienced stress as a factor that may impact on its execution, thereby leading to impaired performance. Thirty elderly and thirty young participants completed a version of the Flanker task paired with electroencephalographic recordings of the alpha frequency, whose increased synchronisation indexes inhibitory processes. Among high stress elderly individuals, findings revealed a general slowing of reaction times for congruent and incongruent stimuli, which correlated with alpha desynchronisation for both stimulus categories. Results found high performing (low stress) elderly revealed neither a behavioural nor electrophysiological difference compared to young participants. Therefore, rather than impacting on top-down compensatory mechanisms, findings indicate that stress may affect elderly participants' inhibitory control in attentional and sensorimotor domains.

The impact of experienced stress on aged spatial discrimination: Cortical overreliance as a result of hippocampal impairment.

A large body of neuroscientific work indicates that exposure to experienced stress causes damage to both cortical and hippocampal cells and results in impairments to cognitive abilities associated with these structures. Similarly, work within the domain of cognitive aging demonstrates that elderly participants who report experiencing greater amounts of stress show reduced levels of cognitive functioning. The present article attempted to combine both findings by collecting data from elderly and young participants who completed a spatial discrimination paradigm developed by Reagh and colleagues [Reagh et al. (2013) Hippocampus 24:303-314] to measure hippocampal-mediated cognitive processes. In order to investigate the effect of stress on the cortex and, indirectly, the hippocampus, it paired the paradigm with electroencephalographic recordings of the theta frequency band, which is thought to reflect cortical/hippocampal interactions. Findings revealed that elderly participants with high levels of experienced stress performed significantly worse on target recognition and lure discrimination and demonstrated heightened levels of cortical theta synchronization compared with young and elderly low stress counterparts. Results therefore provided further evidence for the adverse effect of stress on cognitive aging and indicate that impaired behavioral performance among high stress elderly may coincide with an overreliance on cortical cognitive processing strategies as a result of early damage to the hippocampus.

The effects of long-term stress exposure on aging cognition: a behavioral and EEG investigation.

A large field of research seeks to explore and understand the factors that may cause different rates of age-related cognitive decline within the general population. However, the impact of experienced stress on the human aging process has remained an under-researched possibility. This study explored the association between cumulative stressful experiences and cognitive aging, addressing whether higher levels of experienced stress correlate with impaired performance on 2 working memory tasks. Behavioral performance was paired with electroencephalographic recordings to enable insight into the underlying neural processes impacted on by cumulative stress. Thus, the electroencephalogram was recorded while both young and elderly performed 2 different working memory tasks (a Sternberg and N-back paradigm), and cortical oscillatory activity in the theta, alpha, and gamma bandwidths was measured. Behavioral data indicated that a higher stress score among elderly participants related to impaired performance on both tasks. Electrophysiological findings revealed a reduction in alpha and gamma event-related synchronization among high-stress-group elderly participants, indicating that higher levels of experienced stress may impact on their ability to actively maintain a stimulus in working memory and inhibit extraneous information interfering with successful maintenance. Findings provide evidence that cumulative experienced stress adversely affects cognitive aging.