Abstract
Abstract. Heart rate variability (HRV) has been linked to effective functioning of prefrontal-subcortical inhibitory circuits. Despite the recognized role of the prefrontal cortex (PFC) in executive functions linked to inhibitory capacity, studies linking HRV to executive functions are inconsistent, likely due to potential confounders. The present study sought to examine this relation in a sample of 50 healthy participants (31 females; Mage = 24.2 years) who underwent assessment of resting HRV and two executive tasks assessing inhibitory control, namely the Rule Shift Cards and the Hayling Sentence Completion Test. Hierarchical multiple regressions showed that HRV predicted performance on both tasks (i.e., time taken to inhibit a strongly activated response) above and beyond the role of sex, body mass index, and impulsivity. Present results disconfirm that the HRV-executive function association is only due to confounders, and corroborate such relationship with the use of two ecological tasks assessing inhibitory control. Current findings support the Neurovisceral Integration Model and provide plausible explanation for previous inconsistent results.
References
2016). Executive functions improvement following a 5-month aquaerobics program in older adults: Role of cardiac vagal control in inhibition performance. Biological Psychology, 115, 69–77. https://doi.org/10.1016/j.biopsycho.2016.01.010
(2010). Increased heart rate variability and executive performance after aerobic training in the elderly. European Journal of Applied Physiology, 109, 617–624. https://doi.org/10.1007/s00421-010-1393-y
(2009). The relationships of impulsivity and cardiovascular responses: The role of gender and task type. International Journal of Psychophysiology, 73, 369–376. https://doi.org/10.1016/j.ijpsycho.2009.05.014
(2000). The relationships of resting baroreflex sensitivity, heart rate variability and measures of impulse control in children and adolescents. International Journal of Psychophysiology, 37, 185–194. https://doi.org/10.1016/S0167-8760(00)00089-1
(2014). Taratura Italiana della Batteria per la valutazione della Sindrome Disesecutiva: BADS
([Italian validation of the Behavioural Assessment of the Dysexecutive Syndrome: BADS] . Firenze, Italy: Organizzazioni Speciali.2016). Prefrontal cortex and impulsivity: Interest of noninvasive brain stimulation. Neuroscience and Biobehavioral Reviews, 71, 112–134. https://doi.org/10.1016/j.neubiorev.2016.08.028
(2008). The association between heart rate variability and cognitive impairment in middle-aged men and women. The Whitehall II Cohort study. Neuroepidemiology, 31, 115–121. https://doi.org/10.1159/000148257
(2016). Age-related differences and heterogeneity in executive functions: Analysis of NAB Executive Functions Module Scores. Archives in Clinical Neuropsychology, 31, 254–262. https://doi.org/10.1093/arclin/acw005
(1997). The Hayling and Brixton Tests. Test manual. Bury St Edmunds, UK: Thames Valley Test Company.
(2015). Age differences in high frequency phasic heart rate variability and performance response to increased executive function load in three executive function tasks. Frontiers in Psychology, 5, 1470. https://doi.org/10.3389/fpsyg.2014.01470
(2013). Executive functions. Annual Review of Psychology, 64, 135–168. https://doi.org/10.1146/annurev-psych-113011-143750
(2009). Relationships between features of autonomic cardiovascular control and cognitive performance. Biological Psychology, 81, 110–117. https://doi.org/10.1016/j.biopsycho.2009.03.003
(2009). Ecological assessment of executive functions in mild cognitive impairment and mild Alzheimer’s disease. Journal of the International Neuropsychological Society: JINS, 15, 751–757. https://doi.org/10.1017/S135561770999035X
(2014). Executive functions, impulsivity, and inhibitory control in adolescents: A structural equation model. Advances in Cognitive Psychology, 10, 32–38. https://doi.org/10.5709/acp-0154-5
(2015). The prefrontal cortex (5th ed.). London, UK: Elsevier.
(2016). Association between attention and heart rate fluctuations in pathological worriers. Frontiers in Neuroscience, 10, 648. https://doi.org/10.3389/fnhum.2016.00648
(2014). Heart rate variability predicts control over memory retrieval. Psychological Science, 25, 458–465. https://doi.org/10.1177/0956797613508789
(2015). Individual differences in resting heart rate variability moderate thought suppression success. Psychophysiology, 52, 1149–1160. https://doi.org/10.1111/psyp.12443
(2004). Heart rate variability and its relation to prefrontal cognitive function: The effects of training and detraining. European Journal of Applied Physiology, 93, 263–272. https://doi.org/10.1007/s00421-004-1208-0
(2003). Vagal influence on working memory and attention. International Journal of Psychophysiology, 48, 263–274. https://doi.org/10.1016/S0167-8760(03)00073-4
(2012). The relationships among heart rate variability, executive functions, and clinical variables in patients with panic disorder. International Journal of Psychophysiology, 86, 269–275. https://doi.org/10.1016/j.ijpsycho.2012.10.004
(2013).
(Executive function: Development, individual differences, and clinical insights . In J. RubensteinP. RakicEds., Neural circuit development and function in the brain (pp. 429–445). London, UK: Academic Press.2015). Focusing neurovisceral integration: Cognition, heart rate variability, and cerebral blood flow. Psychophysiology, 52, 214–224. https://doi.org/10.1111/psyp.12319
(1992). Alternate cardiovascular baseline assessment techniques: Vanilla or resting baseline. Psychophysiology, 29, 742–750. https://doi.org/10.1111/j.1469-8986.1992.tb02052.x
(2003). Attentional and physiological characteristics of patients with dental anxiety. Journal of Anxiety Disorders, 17, 75–87. https://doi.org/10.1016/S0887-6185(02)00178-0
(2016). Insulin resistance and carotid intima-media thickness mediate the association between resting-state heart rate variability and executive function: A path modelling study. Biological Psychology, 117, 216–224. https://doi.org/10.1016/j.biopsycho.2016.04.006
(2013). The association of cardiac vagal control and executive functioning – Findings from the MIDUS study. Journal of Psychiatry Research, 47, 628–635. https://doi.org/10.1016/j.jpsychires.2013.01.018
(2010). Inhibitory control and psychopathology: A meta-analysis of studies using the stop signal task. Journal of the International Neuropsychological Society, 16, 1064–1076. https://doi.org/10.1017/S1355617710000895
(2015). The impact of transcranial direct current stimulation on inhibitory control in young adults. Brain and Behavior, 5, e00332. https://doi.org/10.1002/brb3.332
(1997). Impulsivity and inhibitory control. Psychological Science, 8, 60–64. https://doi.org/10.1111/j.1467-9280.1997.tb00545.x
(2009). Heart rate variability and cognitive function: Effects of physical effort. Biological Psychology, 82, 164–168. https://doi.org/10.1016/j.biopsycho.2009.07.007
(2016). Alterations in amygdala-prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biological Psychiatry, 80, 786–795. https://doi.org/10.1016/j.biopsych.2015.10.013
(2017). A meta-analysis of non-invasive brain stimulation and autonomic functioning: Implications for brain-heart pathways to cardiovascular disease. Neuroscience and Biobehavioral Reviews, 74, 330–341. https://doi.org/10.1016/j.neubiorev.2016.05.001
(2015). Integrating affective and cognitive correlates of heart rate variability: A structural equation modeling approach. International Journal of Psychophysiology, 98, 76–86. https://doi.org/10.1016/j.ijpsycho.2015.07.003
(2010). Autonomic predictors of Stroop performance in young and middle-aged adults. International Journal of Psychophysiology, 76, 123–129. https://doi.org/10.1016/j.ijpsycho.2010.02.007
(1998). Executive and motivational control of performance task behavior, and autonomic heart-rate regulation in children: Physiologic validation of two-factor solution inhibitory control. Journal of Child Psychology and Psychiatry, 39, 525–531. https://doi.org/10.1111/1469-7610.00348
(2012). The nature and organization of individual differences in executive functions: Four general conclusions. Current Directions in Psychological Science, 21, 8–14. https://doi.org/10.1177/0963721411429458
(2011). A unified framework for inhibitory control. Trends in Cognitive Sciences, 15, 453–459. https://doi.org/10.1016/j.tics.2011.07.011
(2015). Evaluation of the beat-to-beat detection accuracy of PulseOn wearable optical heart rate monitor. Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2015, 8099–8102. https://doi.org/10.1109/EMBC.2015.7320273
(2014). When tonic cardiac vagal tone predicts changes in phasic vagal tone: The role of fear and perceptual load. Psychophysiology, 51, 419–426. https://doi.org/10.1111/psyp.12186
(1995). Factor structure of the Barratt Impulsiveness Scale. Journal of Clinical Psychology, 51, 768–774.
(2001). Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: Effects of various respiratory patterns. Clinical Physiology, 21, 365–376. https://doi.org/10.1046/j.1365-2281.2001.00337.x
(2017). Transcranial direct current stimulation enhances soothing positive affect and vagal tone. Neuropsychologia, 96, 256–261. https://doi.org/10.1016/j.neuropsychologia.2017.01.028
(2001). The polyvagal theory: Phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146. https://doi.org/10.1016/S0167-8760(01)00162-3
(2007). The polyvagal perspective. Biological Psychology, 74, 116–143. https://doi.org/10.1016/j.biopsycho.2006.06.009
(2016). Heart rate variability is associated with amygdala functional connectivity with MPFC across younger and older adults. NeuroImage, 139, 44–52. https://doi.org/10.1016/j.neuroimage.2016.05.076
(2017). Normative data for the Hayling and Brixton tests in an Italian population. Archives of Clinical Neuropsychology. Advance online publication. https://doi.org/10.1093/arclin/acx072
(2017). Obesity is associated with lack of inhibitory control and impaired heart rate variability reactivity and recovery in response to food stimuli. International Journal of Psychophysiology, 116, 77–84. https://doi.org/10.1016/j.ijpsycho.2017.04.001
(1994). Cardiac vagal tone and sustained attention in school-age children. Psychophysiology, 31, 17–22. https://doi.org/10.1111/j.1469-8986.1994.tb01020.x
(2014). Kubios HRV – Heart rate variability analysis software. Computer Methods and Programs in Biomedicine, 113, 210–220. https://doi.org/10.1016/j.cmpb.2013.07.024
(2002). An advanced detrending method with application to HRV analysis. IEEE Transactions on Biomedical Engineering, 49, 172–175. https://doi.org/10.1109/10.979357
(1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. Circulation, 93, 1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043
. (2006). On the importance of inhibition: Central and peripheral manifestations of nonlinear inhibitory processes in neural systems. Dose Response, 4, 2–21. https://doi.org/10.2203/dose-response.004.01.002
(2012). A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neuroscience and Biobehavioral Reviews, 36, 747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009
(2009). Heart rate variability, prefrontal neural function and cognitive performance: The neurovisceral integration perspective on self-regulation, adaptation, and health. Annals of Behavioral Medicine, 37, 141–153. https://doi.org/10.1007/s12160-009-9101-z
(2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201–216. https://doi.org/10.1016/S0165-0327(00)00338-4
(2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Biobehavioral Review, 33, 81–88. https://doi.org/10.1016/j.neubiorev.2008.08.004
(2001). The five factor model and impulsivity: Using a structural model of personality to understand impulsivity. Personality and Individual Differences, 30, 669–689. https://doi.org/10.1016/S0191-8869(00)00064-7
(2016). Resting cardiac vagal tone predicts intraindividual reaction time variability during an attention task in a sample of young and healthy adults. Psychophysiology, 53, 1843–1851. https://doi.org/10.1111/psyp.12739
(1996). Behavioural assessment of the dysexecutive syndrome. Bury St. Edmunds, UK: Thames Valley Test Company.
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