Impact of cardiac interoception cues and confidence on voluntary decisions to make or withhold action in an intentional inhibition task

Rae, Charlotte L.; Ahmad, Aysha; Larsson, Dennis E O; Silva, Marta; Praag, Cassandra Gould van; Garfinkel, Sarah N.; Critchley, Hugo

doi:10.1038/s41598-020-60405-8

Cited by 25 publications

(19 citation statements)

References 69 publications

(96 reference statements)

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“…More recently, Rae et al have reported mixed findings regarding the impact of cardiac signal on intentional inhibition: although decisions to make or withhold actions seemed not to be influenced by cardiac phase, lower insight into bodily signals was linked to urges to move the body. The authors have suggested that reactive behaviour might result from noisy evidence that increases drift rate, and tips accumulators for execution of action towards motor threshold 42 . Interestingly, our results shed light on an alternative hypothesis in providing experimental evidence that processing bodily information might foster reactive behaviour through a less conservative response criterion for decision-making.…”

Section: Discussionmentioning

confidence: 99%

Environment and body-brain interplay affect inhibition and decision-making

Bouny¹,

Trousselard

Jacob³

et al. 2022

Sci Rep

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The fine-tuned interplay of brain and body underlies human ability to cope with changes in the internal and external milieus. Previous research showed that cardiac interoceptive changes (e.g., cardiac phase) affect cognitive functions, notably inhibition that is a key element for adaptive behaviour. Here we investigated the influence on cognition of vestibular signal, which provides the brain with sensory information about body position and movement. We used a centrifuge-based design to disrupt vestibular signal in healthy human volunteers while their inhibition and decision-making functions were assessed with the stop-signal paradigm. Participants performed the standard and a novel, sensorial version of the stop-signal task to determine whether disrupted vestibular signal influences cognition as a function of its relevance to the context. First, we showed that disrupted vestibular signal was associated with a larger variability of longest inhibition latencies, meaning that participants were even slower to inhibit in the trials where they had the most difficulty inhibiting. Second, we revealed that processing of bodily information, as required in the sensorial stop-signal task, also led to a larger variability of longest inhibition latencies, which was all the more important when vestibular signal was disrupted. Lastly, we found that such a degraded response inhibition performance was due in part to the acceleration of decision-making process, meaning that participants made a decision more quickly even when strength of sensory evidence was reduced. Taken together, these novel findings provide direct evidence that vestibular signal affects the cognitive functions of inhibition and decision-making.

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Section: Discussionmentioning

confidence: 99%

Environment and body-brain interplay affect inhibition and decision-making

Bouny¹,

Trousselard

Jacob³

et al. 2022

Sci Rep

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“…1 ). Green Go cues indicated a button press to be made with the right index finger, red NoGo cues indicated the participant should withhold their button press and yellow ‘Choose’ cues indicated participants should choose whether to press the button or withhold ( Rae et al ., 2020 ). There were 864 trials: 432 Go (50%), 144 NoGo (17%) and 288 Choose (33%), presented in a pseudo-randomized order.…”

Section: Methodsmentioning

confidence: 99%

“…There were 864 trials: 432 Go (50%), 144 NoGo (17%) and 288 Choose (33%), presented in a pseudo-randomized order. The higher frequency of Go trials was designed to invoke a pre-potent tendency to go, as in traditional Go/NoGo tasks and ensure that withholding on NoGo trials was sufficiently challenging to invoke inhibitory control ( Rae et al ., 2020 ). Participants were instructed to respond quickly on Go trials, withhold button presses on NoGo trials and choose quickly, making a fresh decision each time, on Choose trials.…”

Section: Methodsmentioning

confidence: 99%

“…In addition, we used a modified Go/NoGo task, to incorporate ‘Choose’ trials, when participants chose whether to act or to withhold a button press ( Rae et al ., 2020 ). This allowed simultaneous investigation of voluntary action (on Choose trials when participants elected to act), intentional inhibition (on Choose trials when participants elected to withhold) and reactive inhibition (on NoGo trials).…”

Section: Introductionmentioning

confidence: 99%

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Amplified engagement of prefrontal cortex during control of voluntary action in Tourette syndrome

Rae

Parkinson

Betka

et al. 2020

Brain Communications

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Tourette syndrome is characterised by ‘unvoluntary’ tics, which are compulsive, yet often temporarily suppressible. The inferior frontal gyrus (IFG) is implicated in motor control, including inhibition of pre-potent actions through influences on downstream subcortical and motor regions. While tic suppression in Tourette Syndrome also engages the IFG, it is unclear whether such prefrontal control of action is also dysfunctional: Tic suppression studies do not permit comparison with control groups, and neuroimaging studies of motor inhibition can be confounded by the concurrent expression or suppression of tics. Here, patients with Tourette syndrome were directly compared to control participants when performing an intentional inhibition task during fMRI. Tic expression was recorded throughout for removal from statistical models. Participants were instructed to make a button press in response to Go cues, withheld responses to NoGo cues to, and decide whether to press or withhold to ‘Choose’ cues. Overall performance was similar between groups, for both intentional inhibition rates (% Choose-Go) and reactive NoGo inhibition commission errors. A subliminal face prime elicited no additional effects on intentional or reactive inhibition. Across participants, the task activated prefrontal and motor cortices and subcortical nuclei, including pre-supplementary motor area (preSMA), IFG, insula, caudate nucleus, thalamus, and primary motor cortex. In Tourette syndrome, activity was elevated in the IFG, insula, and basal ganglia, most notably within the right IFG during voluntary action and inhibition (Choose-Go and Choose-NoGo), and reactive inhibition (NoGo-correct). Anatomically, the locus of this IFG hyperactivation during control of voluntary action matched that previously reported for tic suppression. In Tourette syndrome, activity within the caudate nucleus was also enhanced during both intentional (Choose-NoGo) and reactive (NoGo-correct) inhibition. Strikingly, despite the absence of overt motor behaviour, primary motor cortex activity increased in patients with Tourette syndrome but decreased in controls during both reactive and intentional inhibition. Additionally, severity of premonitory sensations scaled with functional connectivity of the preSMA to the caudate nucleus, globus pallidus, and thalamus when choosing to respond (Choose-Go). Together, these results suggest that patients with Tourette syndrome use equivalent prefrontal mechanisms to suppress tics and withhold non-tic actions, but require greater IFG engagement than controls to overcome motor drive from hyperactive downstream regions, notably primary motor cortex. Moreover, premonitory sensations may cue midline motor regions to generate tics through interactions with the basal ganglia.

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“…Thus, significant noise poses a problem for out-of-laboratory applications, as point estimates can contain large errors from technological limitations and motion artifacts within windows of extraction. In experimental psychology, noise has often been dealt with through visual inspection of data (Makovac et al, 2016b;Rae et al, 2020); however, when approaching time courses in relatively larger-scale samples, manual outlier detection is not a pragmatic solution.…”

mentioning

confidence: 99%

RapidHRV: an open-source toolbox for extracting heart rate and heart rate variability

Kirk¹,

Garfinkel²,

Robinson³

2021

Preprint

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Heart rate and its variability have enabled insight into a myriad of psychophysiological phenomena. There is now an influx of research attempting using these metrics within both laboratory settings (typically derived through electrocardiography or pulse oximetry) and ecologically-rich contexts (via wearable photoplethysmography, i.e. smartwatches). However, these signals can be prone to artifacts and a low signal to noise ratio, which traditionally are detected and removed through visual inspection. Here, we developed an open-source Python package, RapidHRV, dedicated to the preprocessing, analysis, and visualization of time-domain heart rate and heart rate variability. Each of these modules can be executed with one line of code and includes automated cleaning. In simulated data, RapidHRV demonstrated excellent recovery of heart rate across most levels of noise (>= 10dB) and moderate-to-excellent recovery of heart rate variability even at relatively low signal to noise ratios (>=20dB) and sampling rates (>=20Hz). Validation in real datasets shows good-to-excellent recovery of heart rate and heart rate variability in electrocardiography and pulse oximetry recordings. Validation in real photoplethysmography demonstrated RapidHRV estimations were sensitive to heart rate and its variability under low motion conditions, but estimates were less stable under higher movement settings.

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Impact of cardiac interoception cues and confidence on voluntary decisions to make or withhold action in an intentional inhibition task

Cited by 25 publications

References 69 publications

Environment and body-brain interplay affect inhibition and decision-making

Environment and body-brain interplay affect inhibition and decision-making

Amplified engagement of prefrontal cortex during control of voluntary action in Tourette syndrome

RapidHRV: an open-source toolbox for extracting heart rate and heart rate variability

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