Pupillary Response and Brain Mechanisms of Cognitive Control

doi:10.16719/j.cnki.1671-6981.20240101

Abstract

Abstract: Cognitive control which forms the basis of goal-oriented behavior, is closely related to people's daily life, learning, and work, and is a hot topic in the fields of psychology and neuroscience. Pupillometry provides a new perspective on cognitive control. The pupillary response can be divided into two components: tonic pupil size and phasic pupil response. Tonic pupil size usually refers to baseline pupil size, and phasic pupil response corresponds to task-evoked pupillary response (TEPR). This paper summarizes the relationship between pupillary response and cognitive control, as well as the underlying brain mechanisms of pupillary response induced by cognitive processing.
Few studies have correlated baseline pupil size with cognitive control, and their results are inconsistent. Moreover, there was no definitive evidence of a linear correlation between baseline pupil size and individual differences in cognitive control. Across the domains of inhibition, switching, and updating, TEPR closely responds to changes in task demands and cognitive effort. In addition, TEPR can also effectively reflect the individual monitoring of error and conflict, as well as the subsequent cognitive control regulation. Many lines of evidence indicate that TEPR provides an effective online measurement psychophysical marker of effort changes in different cognitive control processing. TEPR is positively correlated with participants’ cognitive control task performance, and in some cases, its magnitude can predict the improvement of task performance. However, the relationship between TEPR and cognitive control task performance is influenced by task difficulty, and this correlation vanishes when the task is easy. Thus, individual differences in cognitive control lie not only in the amount but also in the efficiency of cognitive effort exerted, which can be reflected in the TEPR.
Collectively, prior research has suggested that pupil response can be used as an indirect indicator of locus coeruleus-norepinephrine (LC-NE) system activity. The combination of EEG or fMRI with pupillometry revealed that the LC-NE system may play different roles in different cognitive control subprocesses. Specifically, the LC-NE system may mainly be responsible for amplifying the gain of relevant information and suppressing irrelevant information in task switching, whereas regulating the motion response process in inhibition tasks. Thus, individual differences in cognitive control are probably related to differences in LC-NE function.
Future research could focus on the following aspects. Firstly, various pupillary indexes have been used in different studies, making it difficult to compare between studies. Thus, it is necessary to explore a more sensitive and effective pupillary activity index suitable for cognitive control research and optimize the analysis of pupil data. Secondly, the relationship between baseline pupil size and cognitive control is still unclear. A systematic study is necessary to investigate the relationships between baseline pupil size as well as the variability of baseline pupil size with cognitive control capacity, with consideration of confounding factors and nonlinear correlations. Thirdly, taking advantage of the higher temporal resolution of TEPR to reveal the temporal dynamic processing of cognitive control. Finally, other techniques (e.g., EEG, fMRI, or machine learning) can be combined with pupillometry to advance the understanding of the complex role of brain mechanisms, especially the LC-NE system in cognitive control processing.

Key words: cognitive control, baseline pupil size, TEPR, LC-NE

摘要： 瞳孔反应包括基线瞳孔大小和任务诱发瞳孔反应,基线瞳孔大小与认知控制的关系仍未确定,任务诱发瞳孔反应可以反映不同认知控制加工中认知努力的变化,且与个体的认知控制成绩正相关。瞳孔反应与蓝斑-去甲肾上腺素系统的活性相关,该系统在不同的认知控制中发挥不同的作用。后续研究可以进一步探讨瞳孔反应与认知控制个体差异的关系,利用瞳孔测量的较高时间分辨率揭示认知控制的时间动态特征,结合其他技术手段探究认知控制的脑机制。

关键词: 认知控制, 基线瞳孔大小, TEPR, LC-NE

Wang Zhijing, Li Fuhong. Pupillary Response and Brain Mechanisms of Cognitive Control[J]. Journal of Psychological Science, 2024, 47(1): 2-10.

王志静, 李富洪. 认知控制的瞳孔反应及脑机制^*[J]. 心理科学, 2024, 47(1): 2-10.

References

[1] 陈安涛. (2019). 认知控制基本功能的神经机制. 生理学报, 71(1), 149-155.
[2] 陆润豪, 张兴利, 施建农. (2021). 眼动技术在个体认知能力差异研究中的应用. 心理科学, 44(3), 552-558.
[3] 杨晓梦, 王福兴, 王燕青, 赵婷婷, 高春颍, 胡祥恩. (2020). 瞳孔是心灵的窗口吗?——瞳孔在心理学研究中的应用及测量. 心理科学进展, 28(7), 1029-1041.
[4] Aminihajibashi S., Hagen T., Andreassen O. A., Laeng B., & Espeseth T. (2020). The effects of cognitive abilities and task demands on tonic and phasic pupil sizes. Biological Psychology, 156, Article 107945.
[5] Aminihajibashi S., Hagen T., Foldal M. D., Laeng B., & Espeseth T. (2019). Individual differences in resting-state pupil size: Evidence for association between working memory capacity and pupil size variability. International Journal of Psychophysiology, 140, 1-7.
[6] Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403-450.
[7] Beatty J.,& Lucero-Wagoner, B. (2000). The pupillary system. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (pp. 142-162). Cambridge University Press.
[8] Chmielewski W. X., Mückschel M., Ziemssen T., & Beste C. (2017). The norepinephrine system affects specific neurophysiological subprocesses in the modulation of inhibitory control by working memory demands. Human Brain Mapping, 38(1), 68-81.
[9] Critchley H. D., Tang J., Glaser D., Butterworth B., & Dolan R. J. (2005). Anterior cingulate activity during error and autonomic response. NeuroImage, 27(4), 885-895.
[10] da Silva Castanheira K., LoParco S., & Otto A. R. (2021). Task-evoked pupillary responses track effort exertion: Evidence from task-switching. Cognitive, Affective, and Behavioral Neuroscience, 21(3), 592-606.
[11] Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64, 135-168.
[12] Diede, N. T., & Bugg, J. M. (2017). Cognitive effort is modulated outside of the explicit awareness of conflict frequency: Evidence from pupillometry. Journal of Experimental Psychology: Learning, Memory, and Cognition, 43(5), 824-835.
[13] Dippel G., Mückschel M., Ziemssen T., & Beste C. (2017). Demands on response inhibition processes determine modulations of theta band activity in superior frontal areas and correlations with pupillometry - Implications for the norepinephrine system during inhibitory control. NeuroImage, 157, 575-585.
[14] Duchowski A. T., Krejtz K., Gehrer N. A., Bafna T., & Bækgaard P. (2020). The low/high index of pupillary activity. Poster session presented at 2020 CHI conference on human factors in computing systems, Honolulu, HI, USA.
[15] Giller F., Mückschel M., Ziemssen T., & Beste C. (2020). A possible role of the norepinephrine system during sequential cognitive flexibility-Evidence from EEG and pupil diameter data. Cortex, 128, 22-34.
[16] Grueschow M., Kleim B., & Ruff C. C. (2020). Role of the locus coeruleus arousal system in cognitive control. Journal of Neuroendocrinology, 32(12), Article e12890.
[17] Hershman R., Levin Y., Tzelgov J., & Henik A. (2021). Neutral stimuli and pupillometric task conflict. Psychological Research, 85(3), 1084-1092.
[18] Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143(3611), 1190-1192.
[19] Hjortkjær J., Märcher-Rørsted J., Fuglsang S. A., & Dau T. (2020). Cortical oscillations and entrainment in speech processing during working memory load. European Journal of Neuroscience, 51(5), 1279-1289.
[20] Hsu Y. F., Baird T., & Wang C. A. (2020). Investigating cognitive load modulation of distractor processing using pupillary luminance responses in the anti-saccade paradigm. European Journal of Neuroscience, 52(3), 3061-3073.
[21] Isabella S. L., Urbain C., Cheyne J. A., & Cheyne D. (2019). Pupillary responses and reaction times index different cognitive processes in a combined Go/Switch incidental learning task. Neuropsychologia, 127, 48-56.
[22] Jodoj E., Chiang C., & Aston-Jones G. (1998). Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons. Neuroscience, 83(1), 63-79.
[23] Joshi, S., & Gold, J. I. (2020). Pupil size as a window on neural substrates of cognition. Trends in Cognitive Sciences, 24(6), 466-480.
[24] Joshi S., Li Y., Kalwani R. M., & Gold J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89(1), 221-234.
[25] Karatekin C., Bingham C., & White T. (2009). Regulation of cognitive resources during an n-back task in youth-onset psychosis and attention-deficit/hyperactivity disorder (ADHD). International Journal of Psychophysiology, 73(3), 294-307.
[26] Katidioti I., Borst J. P., & Taatgen N. A. (2014). What happens when we switch tasks: Pupil dilation in multitasking. Journal of Experimental Psychology: Applied, 20(4), 380-396.
[27] Krejtz K., Duchowski A. T., Niedzielska A., Biele C., & Krejtz I. (2018). Eye tracking cognitive load using pupil diameter and microsaccades with fixed gaze. PLoS ONE, 13(9), Article e0203629.
[28] Laeng B., Ørbo M., Holmlund T., & Miozzo M. (2011). Pupillary Stroop effects. Cognitive Processing, 12(1), 13-21.
[29] Maier M. E., Ernst B., & Steinhauser M. (2019). Error-related pupil dilation is sensitive to the evaluation of different error types. Biological Psychology, 141, 25-34.
[30] Mathôt, S. (2018). Pupillometry: Psychology, physiology, and function. Journal of Cognition, 1(1), Article 16.
[31] Miyake A., Friedman N. P., Emerson M. J., Witzki A. H., Howerter A., & Wager T. D. (2000). The unity and diversity of executive functions and their contributions to complex "Frontal Lobe" tasks: A latent variable analysis. Cognitive Psychology, 41(1), 49-100.
[32] Mückschel M., Chmielewski W., Ziemssen T., & Beste C. (2017). The norepinephrine system shows information-content specific properties during cognitive control - Evidence from EEG and pupillary responses. NeuroImage, 149, 44-52.
[33] Muller T. H., Mars R. B., Behrens T. E., & O'Reilly J. X. (2019). Control of entropy in neural models of environmental state. eLife, 8, Article e39404.
[34] Pajkossy P., Szőllősi Á., Demeter G., & Racsmány M. (2017). Tonic noradrenergic activity modulates explorative behavior and attentional set shifting: Evidence from pupillometry and gaze pattern analysis. Psychophysiology, 54(12), 1839-1854.
[35] Pajkossy P., Szőllősi Á., Demeter G., & Racsmány M. (2018). Physiological measures of dopaminergic and noradrenergic activity during attentional set shifting and reversal. Frontiers in Psychology, 9, Article 506.
[36] Peinkhofer C., Knudsen G. M., Moretti R., & Kondziella D. (2019). Cortical modulation of pupillary function: Systematic review. PeerJ, 7, Article e6882.
[37] Peysakhovich V., Vachon F., & Dehais F. (2017). The impact of luminance on tonic and phasic pupillary responses to sustained cognitive load. International Journal of Psychophysiology, 112, 40-45.
[38] Rondeel E. W. M., van Steenbergen H., Holland R. W., & van Knippenberg A. (2015). A closer look at cognitive control: Differences in resource allocation during updating, inhibition and switching as revealed by pupillometry. Frontiers in Human Neuroscience, 9, Article 494.
[39] Schriver B. J., Perkins S. M., Sajda P., & Wang Q. (2020). Interplay between components of pupil-linked phasic arousal and its role in driving behavioral choice in Go/No-Go perceptual decision-making. Psychophysiology, 57(8), Article e13565.
[40] Tsukahara, J. S., & Engle, R. W. (2021). Is baseline pupil size related to cognitive ability? Yes (under proper lighting conditions). Cognition, 211, Article 104643.
[41] Tsukahara J. S., Harrison T. L., & Engle R. W. (2016). The relationship between baseline pupil size and intelligence. Cognitive Psychology, 91, 109-123.
[42] Unsworth, N., & Robison, M. K. (2017a). A locus coeruleus-norepinephrine account of individual differences in working memory capacity and attention control. Psychonomic Bulletin and Review, 24(4), 1282-1311.
[43] Unsworth, N., & Robison, M. K. (2017b). The importance of arousal for variation in working memory capacity and attention control: A latent variable pupillometry study. Journal of Experimental Psychology: Learning, Memory, and Cognition, 43(12), 1962-1987.
[44] Unsworth, N., & Robison, M. K. (2018). Tracking working memory maintenance with pupillometry. Attention, Perception, and Psychophysics, 80(2), 461-484.
[45] Unsworth N., Miller A. L., & Robison M. K. (2021a). Is working memory capacity related to baseline pupil diameter? Psychonomic Bulletin and Review, 28(1), 228-237.
[46] Unsworth N., Miller A. L., & Robison M. K. (2021b). No consistent correlation between baseline pupil diameter and cognitive abilities after controlling for confounds-A comment on Tsukahara and Engle (2021). Cognition, 215, Article 104825.
[47] Unsworth N., Robison M. K., & Miller A. L. (2019). Individual differences in baseline oculometrics: Examining variation in baseline pupil diameter, spontaneous eye blink rate, and fixation stability. Cognitive, Affective, and Behavioral Neuroscience, 19(4), 1074-1093.
[48] van der Wel, P., & van Steenbergen, H. (2018). Pupil dilation as an index of effort in cognitive control tasks: A review. Psychonomic Bulletin and Review, 25(6), 2005-2015.
[49] van Rij J., Hendriks P., van Rijn H., Baayen R. H., & Wood S. N. (2019). Analyzing the time course of pupillometric data. Trends in Hearing, 23, Article 2331216519832483.
[50] van Steenbergen, H., & Band, G. P. H. (2013). Pupil dilation in the Simon task as a marker of conflict processing. Frontiers in Human Neuroscience, 7, Article 215.
[51] Varazzani C., San-Galli A., Gilardeau S., & Bouret S. (2015). Noradrenaline and dopamine neurons in the reward/effort trade-off: A direct electrophysiological comparison in behaving monkeys. The Journal of Neuroscience, 35(20), 7866-7877.
[52] Wang C. A., Brien D. C., & Munoz D. P. (2015). Pupil size reveals preparatory processes in the generation of pro-saccades and anti-saccades. European Journal of Neuroscience, 41(8), 1102-1110.
[53] Wang, C. A., & Munoz, D. P. (2021). Coordination of pupil and saccade responses by the superior colliculus. Journal of Cognitive Neuroscience, 33(5), 919-932.
[54] Wolff N., Mückschel M., Ziemssen T., & Beste C. (2018). The role of phasic norepinephrine modulations during task switching: Evidence for specific effects in parietal areas. Brain Structure and Function, 223(2), 925-940.
[55] Yanaoka K., van't Wout F., Saito S., & Jarrold C. (2022). Prior task experience increases 5-year-old children's use of proactive control: Behavioral and pupillometric evidence. Developmental Science, 25(5), Article e13181.
[56] Yu S. J., Ghin F., Mückschel M., Ziemssen T., Stock A. K., & Beste C. (2022). A role of the norepinephrine system or effort in the interplay of different facets of inhibitory control. Neuropsychologia, 166, Article 108143.
[57] Zekveld A. A., van Scheepen, J. A. M., Versfeld N. J., Kramer S. E., & van Steenbergen H. (2020). The influence of hearing loss on cognitive control in an auditory conflict task: Behavioral and pupillometry findings. Journal of Speech, Language, and Hearing Research, 63(7), 2483-2492.