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Motivational and emotional influences on cognitive control in depression: A pupillometry study

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Abstract

Depressed people perform poorly on cognitive tasks; however, under certain conditions they show intact cognitive performance, with physiological reactivity consistent with needing to recruit additional cognitive control. We hypothesized that this apparent compensation is driven by the presence of affective processes (e.g., state anxiety), which in turn are moderated by the depressed individual’s motivational state. Clarifying these processes may help researchers identify targets for treatment that if addressed may improve depressed patients’ cognitive functioning. To test this hypothesis, 36 participants with unipolar depression and 36 never-depressed controls completed a problem-solving task that was modified to elicit anxiety. The participants completed measures of motivation, anxiety, sadness, and rumination, while pupillary responses were continuously measured during problem-solving, as an index of cognitive control. Anxiety increased throughout the task for all participants, whereas both sadness and rumination were decreased during the task. In addition, anxiety more strongly affected planning accuracy in depressed participants than in controls, regardless of the participants’ levels of motivation. In contrast, differential effects of anxiety on pupillary responses were observed as a function of depressed participants’ levels of motivation. Consistent with the behavioral results, less-motivated and anxious depressed participants demonstrated smaller pupillary responses, whereas more highly motivated and anxious depressed participants demonstrated larger pupillary responses than did controls. Strong effects of sadness and rumination on cognitive control in depression were not observed. Thus, we conclude that anxiety inhibits the recruitment of cognitive control in depression and that a depressed individual’s motivational state determines, in part, whether he or she is able to compensate by recruiting additional cognitive control.

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Notes

  1. No significant interactions with time or task difficulty emerged, other than the significant Task Difficulty × Time interaction. Thus, we controlled for these effects when testing the study’s main hypotheses that did not involve time.

References

  • Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage.

    Google Scholar 

  • Bakes, A., Bradshaw, C. M., & Szabadi, E. (1990). Attenuation of the pupillary light reflex in anxious patients. British Journal of Clinical Pharmacology, 30, 377–381.

    Article  PubMed Central  PubMed  Google Scholar 

  • Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91, 276–292.

    Article  PubMed  Google Scholar 

  • Berggren, N., & Derakshan, N. (2013). Attentional control deficits in trait anxiety: Why you see them and why you don’t. Biological Psychology, 92, 440–446.

    Article  PubMed  Google Scholar 

  • Bitsios, P., Szabadi, E., & Bradshaw, C. (2004). The fear-inhibited light reflex: Importance of the anticipation of an aversive event. International Journal of Psychophysiology, 52, 87–95.

    Article  PubMed  Google Scholar 

  • Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45, 602–607.

    Article  PubMed Central  PubMed  Google Scholar 

  • Chiew, K. S., & Braver, T. S. (2013). Temporal dynamics of motivation–cognitive control interactions revealed by high-resolution pupillometry. Frontiers in Psychology, 4, 15. doi:10.3389/fpsyg.2013.00015

    Article  PubMed Central  PubMed  Google Scholar 

  • Chiew, K. S., & Braver, T. S. (2014). Dissociable influences of reward motivation and positive emotion on cognitive control. Cognitive, Affective, & Behavioral Neuroscience, 14, 509–529. doi:10.3758/s13415-014-0280-0

    Article  Google Scholar 

  • Clarke, R., & Johnstone, T. (2013). Prefrontal inhibition of threat processing reduces working memory interference. Frontiers in Human Neuroscience, 7, 228. doi:10.3389/fnhum.2013.00228

    Article  PubMed Central  PubMed  Google Scholar 

  • Critchley, H. D., Tang, J., Glaser, D., Butterworth, B., & Dolan, R. J. (2005). Anterior cingulate activity during error and autonomic response. NeuroImage, 27, 885–895.

    Article  PubMed  Google Scholar 

  • Cyranowski, J. M., Frank, E., Young, E., & Shear, M. (2000). Adolescent onset of the gender difference in lifetime rates of major depression: A theoretical model. Archives of General Psychiatry, 57, 21–27.

    Article  PubMed  Google Scholar 

  • Deckersbach, T., Nierenberg, A. A., Buhlmann, U., Ostacher, M., Dougherty, D., Loh, R., & Sachs, G. S. (2008). The influence of sadness on working memory in bipolar disorder: An fMRI investigation [Abstract]. Bipolar Disorders, 10, 928–942.

    Article  PubMed  Google Scholar 

  • Elliott, R., Baker, S., Rogers, R., O’Leary, D., Paykel, E. S., Frith, C. D., & Sahakian, B. J. (1997). Prefrontal dysfunction in depressed patients performing a complex planning task: A study using positron emission tomography. Psychological Medicine, 27, 931–942.

    Article  PubMed  Google Scholar 

  • Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., & Hirsch, J. (2006). Resolving emotional conflict: A role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron, 51, 871–882. doi:10.1016/j.neuron.2006.07.029

    Article  PubMed  Google Scholar 

  • First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. (1996). Structured clinical interview for DSM-IV Axis I disorders, patient edition (Vol. 20). New York, NY: Biometrics Research Department New York State Psychiatric Institute.

    Google Scholar 

  • Gianaros, P. J., Sheu, L. K., Matthews, K. A., Jennings, J. R., Manuck, S. B., & Hariri, A. R. (2008). Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. Journal of Neuroscience, 28, 990–999.

    Article  PubMed Central  PubMed  Google Scholar 

  • Godard, J., Grondin, S., Baruch, P., & Lafleur, M. F. (2011). Psychosocial and neurocognitive profiles in depressed patients with major depressive disorder and bipolar disorder. Psychiatry Research, 190, 244–252.

    Article  PubMed  Google Scholar 

  • Granholm, E., Asarnow, R. F., Sarkin, A. J., & Dykes, K. L. (1996). Pupillary responses index cognitive resource limitations. Psychophysiology, 33, 457–461.

    Article  PubMed  Google Scholar 

  • Granholm, E., & Steinhauer, S. R. (2004). Pupillometric measures of cognitive and emotional processes. International Journal of Psychophysiology, 52, 1–6.

    Article  PubMed  Google Scholar 

  • Gray, K. C., & Williams, D. E. (1969). Anticipation and stuttering: A pupillographic study. Journal of Speech, Language and Hearing Research, 12, 833–839.

    Article  Google Scholar 

  • Harvey, P.-O., Fossati, P., Pochon, J.-B., Levy, R., LeBastard, G., Lehéricy, S., & Dubois, B. (2005). Cognitive control and brain resources in major depression: An fMRI study using the n-back task. NeuroImage, 26, 860–869.

    Article  PubMed  Google Scholar 

  • Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143, 1190–1192.

    Article  PubMed  Google Scholar 

  • Holmes, A. J., & Pizzagalli, D. A. (2008). Spatiotemporal dynamics of error processing dysfunctions in major depressive disorder. Archives of General Psychiatry, 65, 179–188. doi:10.1001/archgenpsychiatry.2007.19

    Article  PubMed Central  PubMed  Google Scholar 

  • Iwanaga, M., Kobayashi, A., & Kawasaki, C. (2005). Heart rate variability with repetitive exposure to music. Biological Psychology, 70, 61–66. doi:10.1016/j.biopsycho.2004.11.015

    Article  PubMed  Google Scholar 

  • Jones, N. P., Siegle, G. J., Muelly, E. R., Haggerty, A., & Ghinassi, F. (2010). Poor performance on cognitive tasks in depression: Doing too much or not enough? Cognitive, Affective, & Behavioral Neuroscience, 10, 129–140. doi:10.3758/CABN.10.1.129

    Article  Google Scholar 

  • Jones, N. P., Siegle, G. J., Proud, L., Silk, J. S., Hardy, D., Keljo, D. J., & Szigethy, E. (2011). Impact of inflammatory bowel disease and high-dose steroid exposure on pupillary responses to negative information in pediatric depression. Psychosomatic Medicine, 73, 151–157.

    Article  PubMed Central  PubMed  Google Scholar 

  • Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154, 1583–1585.

    Article  PubMed  Google Scholar 

  • Kanske, P., Heissler, J., Schönfelder, S., Bongers, A., & Wessa, M. (2011). How to regulate emotion? neural networks for reappraisal and distraction. Cerebral Cortex, 21, 1379–1388. doi:10.1093/cercor/bhq216

    Article  PubMed  Google Scholar 

  • Kouneiher, F., Charron, S., & Koechlin, E. (2009). Motivation and cognitive control in the human prefrontal cortex. Nature Neuroscience, 12, 939–945.

    Article  PubMed  Google Scholar 

  • Lader, M. (1983). The psychophysiology of anxiety. L’Encéphale, 9(4, Supp. 2), 205B–210B.

    PubMed  Google Scholar 

  • Matsuo, K., Glahn, D. C., Peluso, M. A. M., Hatch, J. P., Monkul, E. S., Najt, P., & Soares, J. C. (2007). Prefrontal hyperactivation during working memory task in untreated individuals with major depressive disorder. Molecular Psychiatry, 12, 158–166. doi:10.1038/sj.mp.4001894

    Article  PubMed  Google Scholar 

  • McLaughlin, K. A., Borkovec, T. D., & Sibrava, N. J. (2007). The effects of worry and rumination on affect states and cognitive activity. Behavior Therapy, 38, 23–38.

    Article  PubMed  Google Scholar 

  • McRae, K., Hughes, B., Chopra, S., Gabrieli, J. D. E., Gross, J. J., & Ochsner, K. N. (2010). The neural bases of distraction and reappraisal. Journal of Cognitive Neuroscience, 22, 248–262. doi:10.1162/jocn.2009.21243

    Article  PubMed Central  PubMed  Google Scholar 

  • Moberly, N. J., & Watkins, E. (2008). Ruminative self-focus and negative affect: An experience sampling study. Journal of Abnormal Psychology, 117, 314–323.

    Article  PubMed Central  PubMed  Google Scholar 

  • Murray, D. C. (1971). Talk, silence and anxiety. Psychological Bulletin, 75, 244–260. doi:10.1037/h0030801

    Article  PubMed  Google Scholar 

  • Nelson, H. E., & Willison, J. R. (1991). National adult reading test (NART): Test manual (2nd ed.). Berkshire, UK: Nfer-Nelson.

    Google Scholar 

  • Nolen-Hoeksema, S., & Morrow, J. (1991). A prospective study of depression and posttraumatic stress symptoms after a natural disaster: The 1989 Loma Prieta earthquake. Journal of Personality and Social Psychology, 61, 115–121.

    Article  PubMed  Google Scholar 

  • Pochon, J. B., Levy, R., Fossati, P., Lehéricy, S., Poline, J. B., Pillon, B., . . . Dubois, B. (2002). The neural system that bridges reward and cognition in humans: An fMRI study. Proceedings of the National Academy of Sciences, 99, 5669–5674. doi:10.1073/pnas.082111099

  • Qin, S., Hermans, E. J., van Marle, H. J. F., Luo, J., & Fernández, G. (2009). Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological Psychiatry, 66, 25–32. doi:10.1016/j.biopsych.2009.03.006

    Article  PubMed  Google Scholar 

  • Rose, E. J., Simonotto, E., & Ebmeier, K. P. (2006). Limbic over-activity in depression during preserved performance on the n-back task. NeuroImage, 29, 203–215.

    Article  PubMed  Google Scholar 

  • Scheurich, A., Fellgiebel, A., Schermuly, I., Bauer, S., Wolfges, R., & Muller, M. J. (2008). Experimental evidence for a motivational origin of cognitive impairment in major depression. Psychological Medicine, 38, 237–246.

    Article  PubMed  Google Scholar 

  • Shallice, T. (1982). Specific impairments of planning. Philosophical Transactions of the Royal Society B, 298, 199–209.

    Article  Google Scholar 

  • Siegle, G. J., Ichikawa, N., & Steinhauer, S. (2008). Blink before and after you think: Blinks occur prior to and following cognitive load indexed by pupillary responses. Psychophysiology, 45, 679–687.

    Article  PubMed  Google Scholar 

  • Siegle, G. J., Steinhauer, S. R., Carter, C. S., Ramel, W., & Thase, M. E. (2003a). Do the seconds turn into hours? Relationships between sustained pupil dilation in response to emotional information and self-reported rumination. Cognitve Therapy and Research, 27, 365–382.

    Article  Google Scholar 

  • Siegle, G. J., Steinhauer, S. R., Friedman, E. S., Thompson, W. S., & Thase, M. E. (2011). Remission prognosis for cognitive therapy for recurrent depression using the pupil: Utility and neural correlates. Biological Psychiatry, 69, 726–733.

    Article  PubMed Central  PubMed  Google Scholar 

  • Siegle, G. J., Steinhauer, S. R., Stenger, V. A., Konecky, R., & Carter, C. S. (2003b). Use of concurrent pupil dilation assessment to inform interpretation and analysis of fMRI data. NeuroImage, 20, 114–124.

    Article  PubMed  Google Scholar 

  • Simpson, H., & Molloy, F. (1971). Effects of audience anxiety on pupil size. Psychophysiology, 8, 491–496.

    Article  PubMed  Google Scholar 

  • Stewart, W. F., Ricci, J. A., Chee, E., Hahn, S. R., & Morganstein, D. (2003). Cost of lost productive work time among US workers with depression. JAMA, 289, 3135–3144.

    Article  PubMed  Google Scholar 

  • Unterrainer, J. M., & Owen, A. M. (2006). Planning and problem solving: From neuropsychology to functional neuroimaging. Journal of Physiology, 99, 308–317.

    PubMed  Google Scholar 

  • Unterrainer, J. M., Rahm, B., Kaller, C. P., Ruff, C. C., Spreer, J., Krause, B. J., & Halsband, U. (2004). When planning fails: Individual differences and error-related brain activity in problem solving. Cerebral Cortex, 14, 1390–1397.

    Article  PubMed  Google Scholar 

  • Van Dillen, L. F., Heslenfeld, D. J., & Koole, S. L. (2009). Tuning down the emotional brain: An fMRI study of the effects of cognitive load on the processing of affective images. NeuroImage, 45, 1212–1219.

    Article  PubMed  Google Scholar 

  • van Tol, M. J., van der Wee, N. J. A., Demenescu, L. R., Nielen, M. M. A., Aleman, A., Renken, R., & Veltman, D. J. (2011). Functional MRI correlates of visuospatial planning in out-patient depression and anxiety. Acta Psychiatrica Scandinavica, 124, 273–284.

    Article  PubMed  Google Scholar 

  • Wagner, G., Sinsel, E., Sobanski, T., Köhler, S., Marinou, V., Mentzel, H.-J., & Schlösser, R. G. M. (2006). Cortical inefficiency in patients with unipolar depression: An event-related fMRI study with the Stroop task. Biological Psychiatry, 59, 958–965. doi:10.1016/j.biopsych.2005.10.025

    Article  PubMed  Google Scholar 

  • Walter, H., Wolf, R. C., Spitzer, M., & Vasic, N. (2007). Increased left prefrontal activation in patients with unipolar depression: An event-related, parametric, performance-controlled fMRI study. Journal of Affective Disorders, 101, 175–185.

    Article  PubMed  Google Scholar 

  • Watkins, E., & Brown, R. G. (2002). Rumination and executive function in depression: An experimental study. Journal of Neurology, Neurosurgery & Psychiatry, 72, 400–402. doi:10.1136/jnnp.72.3.400

    Article  Google Scholar 

  • Whitmer, A. J., & Gotlib, I. H. (2012). Switching and backward inhibition in major depressive disorder: The role of rumination. Journal of Abnormal Psychology, 121, 570–578. doi:10.1037/a0027474

    Article  PubMed  Google Scholar 

  • Wilson, M., Smith, N. C., Chattington, M., Ford, M., & Marple-Horvat, D. E. (2006). The role of effort in moderating the anxiety–performance relationship: Testing the prediction of processing efficiency theory in simulated rally driving. Journal of Sports Sciences, 24, 1223–1233. doi:10.1080/02640410500497667

    Article  PubMed  Google Scholar 

  • Yoshimura, S., Okamoto, Y., Onoda, K., Matsunaga, M., Okada, G., Kunisato, Y., & Yamawaki, S. (2014). Cognitive behavioral therapy for depression changes medial prefrontal and ventral anterior cingulate cortex activity associated with self-referential processing. Social Cognitive and Affective Neuroscience, 9, 487–493. doi:10.1093/scan/nst009

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhu, X., Wang, X., Xiao, J., Liao, J., Zhong, M., Wang, W., & Yao, S. (2012). Evidence of a dissociation pattern in resting-state default mode network connectivity in first-episode, treatment-naive major depression patients. Biological Psychiatry, 71, 611–617. doi:10.1016/j.biopsych.2011.10.035

    Article  PubMed  Google Scholar 

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Author note

This work was supported by National Institute of Mental Health (Grant Nos. MH086811, to N.J., and MH074807 and MH082998, to G.J.S.). The Funders had no role in study design, data collection and analysis, decision to publish, or preparation of the article. We thank Ashley F. McFarland, Olivia L. Conner, and Jillian Rodgers for their role in data collection, as well as the staff of the Mood Disorders Treatment and Research Program at Western Psychiatric Institute and Clinic.

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Correspondence to Neil P. Jones.

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Jones, N.P., Siegle, G.J. & Mandell, D. Motivational and emotional influences on cognitive control in depression: A pupillometry study. Cogn Affect Behav Neurosci 15, 263–275 (2015). https://doi.org/10.3758/s13415-014-0323-6

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