Correlation between LIFG and autonomic activation during stressful tasks: A functional near-infrared spectroscopy (fNIRS) study

Abstract

It remains unclear whether language tasks in one’s first (L1) or second (L2) language can cause stress responses and whether frontal, autonomic and behavioral responses to stressful tasks are correlated. In this study, we studied 22 Chinese subjects whose L2 was English and measured the cerebral blood oxygenation in their frontal lobe by using functional near-infrared spectroscopy (fNIRS) as participants engaged in a mental arithmetic task (MAT) and verbal fluency tasks (VFTs) in L1 (Chinese) and L2 (English). To examine the activated cortical areas, we estimated the channel location based on Montreal Neurological Institute (MNI) standard brain space by using a probabilistic estimation method. We evaluated heart rate (HR) changes to analyze autonomic nervous system (ANS) functioning. We found that the MAT and VFTs induced greater increases in HR than did the control (Ctrl) task. Furthermore, subjects developed greater increases in HR in the MAT and VFT_L2 than they did in the VFT_L1. Compared with the Ctrl task, the MAT and both VFT_L1 and VFT_L2 produced robust and widespread bilateral activation of the frontal cortex. Interestingly, partial correlation analysis indicated that the activity in the left inferior frontal gyrus (LIFG) [Brodmann’s area (BA) 47] was consistently correlated with the increases in HR across the three tasks (MAT, VFT_L2, and VFT_L1), after controlling for the performance data. The present results suggested that a VFT in L2 may be more stressful than in L1. The LIFG may affect the activation of the sympathetic system induced by stressful tasks, including MATs and VFTs.

Keywords

functional near-infrared spectroscopy / mental arithmetic task / verbal fluency task / autonomic nervous system / inferior frontal gyrus

References

[1] LazarusRS. Stress and emotion: A new synthesis, 2006, New York, Springer Publishing Company

[2] BonannoGA. Loss, trauma, and human resilience: have we underestimated the human capacity to thrive after extremely aversive events?. Am Psychol, 2004, 59(1): 20-28 PMID: 14736317

[3] RamachandruniS, HandbergE, ShepsDS. Acute and chronic psychological stress in coronary disease. Curr Opin Cardiol, 2004, 19(5): 494-499 PMID: 15316459

[4] SmeetsT. Autonomic and hypothalamic-pituitary-adrenal stress resilience: Impact of cardiac vagal tone. Biol Psychol, 2010, 84(2): 290-295 PMID: 20206227

[5] CarterJR, RayCA. Sympathetic neural responses to mental stress: responders, nonresponders and sex differences. Am J Physiol Heart Circ Physiol, 2009, 296(3): H847-853 PMID: 19168718 PMCID: 2660243

[6] FoxK, BorerJS, CammAJ, et al. . Resting heart rate in cardiovascular disease. J Am Coll Cardiol, 2007, 50(9): 823-830 PMID: 17719466

[7] JouvenX, SchwartzPJ, EscolanoS, et al. . Excessive heart rate increase during mild mental stress in preparation for exercise predicts sudden death in the general population. Eur Heart J, 2009, 30(14): 1703-1710 PMID: 19401600

[8] FalconeC, BuzziMP, KlersyC, et al. . Rapid heart rate increase at onset of exercise predicts adverse cardiac events in patients with coronary artery disease. Circulation, 2005, 112(13): 1959-1964 PMID: 16172270

[9] WangJ, RaoH, WetmoreGS, et al. . Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc Natl Acad Sci USA, 2005, 102(49): 17804-17809 PMID: 16306271 PMCID: 1292988

[10] CritchleyHD, ElliottR, MathiasCJ, et al. . Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J Neurosci, 2000, 20(8): 3033-3040 PMID: 10751455

[11] LiakakisG, NickelJ, SeitzRJ. Diversity of the inferior frontal gyrus—a meta-analysis of neuroimaging studies. Behav Brain Res, 2011, 225(1): 341-347 PMID: 21729721

[12] OngurD, AnX, PriceJL. Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol, 1998, 401(4): 480-505 PMID: 9826274

[13] OngurD, PriceJL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex, 2000, 10(3): 206-219 PMID: 10731217

[14] UrryHL, van ReekumCM, JohnstoneT, et al. . Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J Neurosci, 2006, 26(16): 4415-4425 PMID: 16624961

[15] DrabantEM, KuoJR, RamelW, et al. . Experiential, autonomic, and neural responses during threat anticipation vary as a function of threat intensity and neuroticism. NeuroImage, 2011, 55(1): 401-410 PMID: 21093595 PMCID: 3031673

[16] OldfieldRC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 1971, 9(1): 97-113 PMID: 5146491

[17] SinghAK, OkamotoM, DanH, et al. . Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI. Neuroimage, 2005, 27(4): 842-851 PMID: 15979346

[18] OkamotoM, DanH, SakamotoK, et al. . Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping. Neuroimage, 2004, 21(1): 99-111 PMID: 14741647

[19] ShattuckDW, MirzaM, AdisetiyoV, et al. . Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage, 2008, 39(3): 1064-1080 PMID: 18037310 PMCID: 2757616

[20] OkamotoM, MatsunamiM, DanH, et al. . Prefrontal activity during taste encoding: an fNIRS study. NeuroImage, 2006, 31(2): 796-806 PMID: 16473020

[21] PalatiniP, PalombaD, BertoloO, et al. . The white-coat effect is unrelated to the difference between clinic and daytime blood pressure and is associated with greater reactivity to public speaking. J Hypertens, 2003, 21(3): 545-553 PMID: 12640248

[22] TanidaM, SakataniK, TakanoR, et al. . Relation between asymmetry of prefrontal cortex activities and the autonomic nervous system during a mental arithmetic task: near infrared spectroscopy study. Neurosci Lett, 2004, 369(1): 69-74 PMID: 15380310

[23] SzirmaiI, AmreinI, PálvölgyiL, et al. . Correlation between blood flow velocity in the middle cerebral artery and EEG during cognitive effort. Cognitive Brain Res, 2005, 24(1): 33-40

[24] FuCH, MorganK, SucklingJ, et al. . A functional magnetic resonance imaging study of overt letter verbal fluency using a clustered acquisition sequence: greater anterior cingulate activation with increased task demand. NeuroImage, 2002, 17(2): 871-879 PMID: 12377161

[25] MacIntyrePD, GardnerRC. Language anxiety: its relationship to other anxieties and to processing in native and second languages. Lang Learn, 1991, 41(4): 513-534

[26] Mueller-PfeifferC, ZeffiroT, O’GormanR, et al. . Cortical and cerebellar modulation of autonomic responses to loud sounds. Psychophysiology, 2014, 51(1): 60-69 PMID: 24016238

[27] OngurD, FerryAT, PriceJL. Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol, 2003, 460(3): 425-449 PMID: 12692859

[28] PattersonJC, UngerleiderLG, BandettiniPA. Task-indpendent functional brain activity correlation with skin conductance changes: an fMRI study. NeuroImage, 2002, 17(4): 1797-1806 PMID: 12498753

[29] FechirM, GamerM, BlasiusI, et al. . Functional imaging of sympathetic activation during mental stress. NeuroImage, 2009, 50(2): 847-854 PMID: 20004250

[30] YoonBW, MorilloCA, CechettoDF, et al. . Cerebral hemispheric lateralization in cardiac autonomic control. Arch Neurol, 1997, 54(6): 741-744 PMID: 9193209

[31] AhernGL, SollersJJ, LaneRD, et al. . Heart rate and heart rate variability changes in the intracarotid sodium amobarbital test. Epilepsia, 2001, 42(7): 912-921 PMID: 11488892

[32] NapadowV, DhondR, ContiG, et al. . Brain correlates of autonomic modulation: combining heart rate variability with fMRI. NeuroImage, 2008, 42(1): 169-177 PMID: 18524629 PMCID: 2603289

[33] TakahashiT, TakikawaY, KawagoeR, et al. . Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task. NeuroImage, 2011, 57(3): 991-1002 PMID: 21600294

[34] CuiX, BrayS, BryantDM, et al. . A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. NeuroImage, 2011, 54(4): 2808-2821 PMID: 21047559 PMCID: 3021967