Literature DB >> 34853084

Respiration, Heartbeat, and Conscious Tactile Perception.

Martin Grund1, Esra Al2,3,4, Marc Pabst2, Alice Dabbagh2,5, Tilman Stephani2,6, Till Nierhaus2,7, Michael Gaebler2,3, Arno Villringer2,3.   

Abstract

Previous studies have shown that timing of sensory stimulation during the cardiac cycle interacts with perception. Given the natural coupling of respiration and cardiac activity, we investigated here their joint effects on tactile perception. Forty-one healthy female and male human participants reported conscious perception of finger near-threshold electrical pulses (33% null trials) and decision confidence while electrocardiography, respiratory activity, and finger photoplethysmography were recorded. Participants adapted their respiratory cycle to expected stimulus onsets to preferentially occur during late inspiration/early expiration. This closely matched heart rate variation (sinus arrhythmia) across the respiratory cycle such that most frequent stimulation onsets occurred during the period of highest heart rate probably indicating highest alertness and cortical excitability. Tactile detection rate was highest during the first quadrant after expiration onset. Interindividually, stronger respiratory phase-locking to the task was associated with higher detection rates. Regarding the cardiac cycle, we confirmed previous findings that tactile detection rate was higher during diastole than systole and newly specified its minimum at 250-300 ms after the R-peak corresponding to the pulse wave arrival in the finger. Expectation of stimulation induced a transient heart deceleration which was more pronounced for unconfident decision ratings. Interindividually, stronger poststimulus modulations of heart rate were linked to higher detection rates. In summary, we demonstrate how tuning to the respiratory cycle and integration of respiratory-cardiac signals are used to optimize performance of a tactile detection task.SIGNIFICANCE STATEMENT Mechanistic studies on perception and cognition tend to focus on the brain neglecting contributions of the body. Here, we investigated how respiration and heartbeat influence tactile perception: respiration phase-locking to expected stimulus onsets corresponds to highest heart rate (and presumably alertness/cortical excitability) and correlates with detection performance. Tactile detection varies across the heart cycle with a minimum when the pulse reaches the finger and a maximum in diastole. Taken together with our previous finding of unchanged early event-related potentials across the cardiac cycle, we conclude that these effects are not a peripheral physiological artifact but a result of cognitive processes that model our body's internal state, make predictions to guide behavior, and might also tune respiration to serve the task.
Copyright © 2022 the authors.

Entities:  

Keywords:  cardiac cycle; electrocardiogram; interoception; photoplethysmography; respiration; tactile perception

Mesh:

Year:  2021        PMID: 34853084      PMCID: PMC8805629          DOI: 10.1523/JNEUROSCI.0592-21.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.709


  47 in total

1.  Cardiovascular and respiratory modulation of tactile afferents in the human finger pad.

Authors:  Vaughan G Macefield
Journal:  Exp Physiol       Date:  2003-09       Impact factor: 2.969

2.  Imperceptible somatosensory stimulation alters sensorimotor background rhythm and connectivity.

Authors:  Till Nierhaus; Norman Forschack; Sophie K Piper; Susanne Holtze; Thomas Krause; Birol Taskin; Xiangyu Long; Johannes Stelzer; Daniel S Margulies; Jens Steinbrink; Arno Villringer
Journal:  J Neurosci       Date:  2015-04-15       Impact factor: 6.167

3.  Heart-rate modulations reveal attention and consciousness interactions.

Authors:  María I Cobos; Pedro M Guerra; Jaime Vila; Ana B Chica
Journal:  Psychophysiology       Date:  2018-10-25       Impact factor: 4.016

4.  Heartbeat detection: judgments of the simultaneity of external stimuli and heartbeats.

Authors:  J Brener; C Kluvitse
Journal:  Psychophysiology       Date:  1988-09       Impact factor: 4.016

5.  Neural correlates of conscious tactile perception: An analysis of BOLD activation patterns and graph metrics.

Authors:  Martin Grund; Norman Forschack; Till Nierhaus; Arno Villringer
Journal:  Neuroimage       Date:  2020-09-17       Impact factor: 6.556

6.  Neural excitability and sensory input determine intensity perception with opposing directions in initial cortical responses.

Authors:  Tilman Stephani; Alice Hodapp; Mina Jamshidi Idaji; Arno Villringer; Vadim V Nikulin
Journal:  Elife       Date:  2021-10-05       Impact factor: 8.140

7.  New approach for T-wave end detection on electrocardiogram: performance in noisy conditions.

Authors:  Carlos R Vázquez-Seisdedos; João Evangelista Neto; Enrique J Marañón Reyes; Aldebaro Klautau; Roberto C Limão de Oliveira
Journal:  Biomed Eng Online       Date:  2011-09-09       Impact factor: 2.819

Review 8.  Interactions between visceral afferent signaling and stimulus processing.

Authors:  Hugo D Critchley; Sarah N Garfinkel
Journal:  Front Neurosci       Date:  2015-08-27       Impact factor: 4.677

9.  Unexpected arousal modulates the influence of sensory noise on confidence.

Authors:  Micah Allen; Darya Frank; D Samuel Schwarzkopf; Francesca Fardo; Joel S Winston; Tobias U Hauser; Geraint Rees
Journal:  Elife       Date:  2016-10-25       Impact factor: 8.140

10.  Respiration aligns perception with neural excitability.

Authors:  Daniel S Kluger; Elio Balestrieri; Niko A Busch; Joachim Gross
Journal:  Elife       Date:  2021-12-14       Impact factor: 8.140

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  3 in total

1.  Respiration-timing-dependent changes in activation of neural substrates during cognitive processes.

Authors:  Nozomu H Nakamura; Masaki Fukunaga; Tetsuya Yamamoto; Norihiro Sadato; Yoshitaka Oku
Journal:  Cereb Cortex Commun       Date:  2022-09-13

Review 2.  Temporal variations in the pattern of breathing: techniques, sources, and applications to translational sciences.

Authors:  Yoshitaka Oku
Journal:  J Physiol Sci       Date:  2022-08-29       Impact factor: 2.257

3.  Rhythms in cognition: The evidence revisited.

Authors:  Christian Keitel; Manuela Ruzzoli; Laura Dugué; Niko A Busch; Christopher S Y Benwell
Journal:  Eur J Neurosci       Date:  2022-06       Impact factor: 3.698

  3 in total

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