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.
Similar content being viewed by others
Notes
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.
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.
Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91, 276–292.
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.
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.
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.
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
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
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
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.
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.
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.
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.
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
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.
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.
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.
Granholm, E., Asarnow, R. F., Sarkin, A. J., & Dykes, K. L. (1996). Pupillary responses index cognitive resource limitations. Psychophysiology, 33, 457–461.
Granholm, E., & Steinhauer, S. R. (2004). Pupillometric measures of cognitive and emotional processes. International Journal of Psychophysiology, 52, 1–6.
Gray, K. C., & Williams, D. E. (1969). Anticipation and stuttering: A pupillographic study. Journal of Speech, Language and Hearing Research, 12, 833–839.
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.
Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143, 1190–1192.
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
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
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
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.
Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154, 1583–1585.
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
Kouneiher, F., Charron, S., & Koechlin, E. (2009). Motivation and cognitive control in the human prefrontal cortex. Nature Neuroscience, 12, 939–945.
Lader, M. (1983). The psychophysiology of anxiety. L’Encéphale, 9(4, Supp. 2), 205B–210B.
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
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.
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
Moberly, N. J., & Watkins, E. (2008). Ruminative self-focus and negative affect: An experience sampling study. Journal of Abnormal Psychology, 117, 314–323.
Murray, D. C. (1971). Talk, silence and anxiety. Psychological Bulletin, 75, 244–260. doi:10.1037/h0030801
Nelson, H. E., & Willison, J. R. (1991). National adult reading test (NART): Test manual (2nd ed.). Berkshire, UK: Nfer-Nelson.
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.
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
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.
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.
Shallice, T. (1982). Specific impairments of planning. Philosophical Transactions of the Royal Society B, 298, 199–209.
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.
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.
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.
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.
Simpson, H., & Molloy, F. (1971). Effects of audience anxiety on pupil size. Psychophysiology, 8, 491–496.
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.
Unterrainer, J. M., & Owen, A. M. (2006). Planning and problem solving: From neuropsychology to functional neuroimaging. Journal of Physiology, 99, 308–317.
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.
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.
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.
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
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.
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
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 76.1 kb)
Rights and permissions
About this article
Cite this article
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
Published:
Issue Date:
DOI: https://doi.org/10.3758/s13415-014-0323-6