When the Heart Inhibits the Brain: Cardiac Phases Modulate Short-interval Intracortical Inhibition

Overview

Journal iScience

Publisher Cell Press

Date 2024 Feb 28

PMID 38414850

Authors

Mario Paci

Pasquale Cardellicchio

Paolo Di Luzio

Mauro Gianni Perrucci

Francesca Ferri

Marcello Costantini

Affiliations

Soon will be listed here.

Abstract

The phasic cardiovascular activity influences the central nervous system through the systolic baroreceptor inputs, inducing widespread inhibitory effects on behavior. Through transcranial magnetic stimulation (TMS) delivered during resting-state over the left primary motor cortex and across the different cardiac phases, we measured corticospinal excitability (CSE) and distinct indices of intracortical motor inhibition: short (SICI) and long (LICI) interval, corresponding to GABA and GABA neurotransmission, respectively. We found a significant effect of the cardiac phase on short-intracortical inhibition, without any influence on LICI. Specifically, SICI was stronger at systole compared to diastole. These results show a tight relationship between the cardiac cycle and the inhibitory neurotransmission within M1, and in particular with GABA-ergic-mediated motor inhibition. We hypothesize that this process requires greater motor control via the gating mechanism and that this, in turn, needs to be recalibrated through the modulation of intracortical inhibition.

References

Vucic S, Cheah B, Krishnan A, Burke D, Kiernan M . The effects of alterations in conditioning stimulus intensity on short interval intracortical inhibition. Brain Res. 2009; 1273:39-47. DOI: 10.1016/j.brainres.2009.03.043. View

Rae C, Botan V, Gould van Praag C, Herman A, Nyyssonen J, Watson D . Response inhibition on the stop signal task improves during cardiac contraction. Sci Rep. 2018; 8(1):9136. PMC: 6002409. DOI: 10.1038/s41598-018-27513-y. View

Greenhouse I, Oldenkamp C, Aron A . Stopping a response has global or nonglobal effects on the motor system depending on preparation. J Neurophysiol. 2011; 107(1):384-92. PMC: 3349702. DOI: 10.1152/jn.00704.2011. View

Silvanto J, Muggleton N, Walsh V . State-dependency in brain stimulation studies of perception and cognition. Trends Cogn Sci. 2008; 12(12):447-54. DOI: 10.1016/j.tics.2008.09.004. View

Hermans L, Maes C, Pauwels L, Cuypers K, Heise K, Swinnen S . Age-related alterations in the modulation of intracortical inhibition during stopping of actions. Aging (Albany NY). 2019; 11(2):371-385. PMC: 6366958. DOI: 10.18632/aging.101741. View

Du X, Summerfelt A, Chiappelli J, Holcomb H, Hong L . Individualized brain inhibition and excitation profile in response to paired-pulse TMS. J Mot Behav. 2013; 46(1):39-48. PMC: 4038908. DOI: 10.1080/00222895.2013.850401. View

Todd J, Cardellicchio P, Swami V, Cardini F, Aspell J . Weaker implicit interoception is associated with more negative body image: Evidence from gastric-alpha phase amplitude coupling and the heartbeat evoked potential. Cortex. 2021; 143:254-266. DOI: 10.1016/j.cortex.2021.07.006. View

Yang X, Jennings J, Friedman B . Exteroceptive stimuli override interoceptive state in reaction time control. Psychophysiology. 2017; 54(12):1940-1950. DOI: 10.1111/psyp.12958. View

Saltafossi M, Zaccaro A, Perrucci M, Ferri F, Costantini M . The impact of cardiac phases on multisensory integration. Biol Psychol. 2023; 182:108642. DOI: 10.1016/j.biopsycho.2023.108642. View

10.

Michalareas G, Vezoli J, van Pelt S, Schoffelen J, Kennedy H, Fries P . Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas. Neuron. 2016; 89(2):384-97. PMC: 4871751. DOI: 10.1016/j.neuron.2015.12.018. View

11.

Cattaneo L, Sandrini M, Schwarzbach J . State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices. Cereb Cortex. 2010; 20(9):2252-8. DOI: 10.1093/cercor/bhp291. View

12.

Paulus W, Classen J, Cohen L, Large C, Di Lazzaro V, Nitsche M . State of the art: Pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimul. 2010; 1(3):151-63. DOI: 10.1016/j.brs.2008.06.002. View

13.

Jacquet P, Avenanti A . Perturbing the action observation network during perception and categorization of actions' goals and grips: state-dependency and virtual lesion TMS effects. Cereb Cortex. 2013; 25(3):598-608. DOI: 10.1093/cercor/bht242. View

14.

Schutter D, Smits F, Klaus J . Mind matters: A narrative review on affective state-dependency in non-invasive brain stimulation. Int J Clin Health Psychol. 2023; 23(3):100378. PMC: 9971283. DOI: 10.1016/j.ijchp.2023.100378. View

15.

Cardellicchio P, Hilt P, Olivier E, Fadiga L, DAusilio A . Early modulation of intra-cortical inhibition during the observation of action mistakes. Sci Rep. 2018; 8(1):1784. PMC: 5788976. DOI: 10.1038/s41598-018-20245-z. View

16.

AMASSIAN V, Cracco R, Maccabee P, Cracco J, Rudell A, Eberle L . Suppression of visual perception by magnetic coil stimulation of human occipital cortex. Electroencephalogr Clin Neurophysiol. 1989; 74(6):458-62. DOI: 10.1016/0168-5597(89)90036-1. View

17.

Tran D, Chowdhury N, McNair N, Harris J, Livesey E . Linking cortical and behavioural inhibition: Testing the parameter specificity of a transcranial magnetic stimulation protocol. Brain Stimul. 2020; 13(5):1381-1383. DOI: 10.1016/j.brs.2020.07.010. View

18.

Duque J, Greenhouse I, Labruna L, Ivry R . Physiological Markers of Motor Inhibition during Human Behavior. Trends Neurosci. 2017; 40(4):219-236. PMC: 5389740. DOI: 10.1016/j.tins.2017.02.006. View

19.

Cardellicchio P, Koch G, Fadiga L, DAusilio A . Motor overload: GABAergic index of parallel buffer costs. Brain Stimul. 2021; 14(5):1106-1108. DOI: 10.1016/j.brs.2021.07.061. View

20.

Roshan L, Paradiso G, Chen R . Two phases of short-interval intracortical inhibition. Exp Brain Res. 2003; 151(3):330-7. DOI: 10.1007/s00221-003-1502-9. View