Altered neural activation during prepotent response inhibition in breast cancer survivors treated with chemotherapy: an fMRI study

Brain Imaging and Behavior

Volumn 10, Issue 3, 2016, Pages 840-848

  Kam, Julia W Y ^a   Boyd, Lara A ^a   Hsu, Chun L ^a   Liu Ambrose, Teresa ^a   Handy, Todd C ^a   Lim, Howard J ^a,b   Hayden, Sherri ^a   Campbell, Kristin L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

Breast cancer survivors; Chemotherapy; Cognitive deficits; Functional MRI; Prepotent response inhibition

Indexed keywords

ANTINEOPLASTIC AGENT; OXYGEN;

ADULT; AGE; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN ANALYSIS; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER SURVIVOR; CANCER THERAPY; CAUDATE NUCLEUS; CINGULATE GYRUS; CLINICAL ARTICLE; COGNITIVE DEFECT; EDUCATIONAL STATUS; EXECUTIVE FUNCTION; EXECUTIVE FUNCTION TEST; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; LINGUAL GYRUS; MIDDLE FRONTAL GYRUS; MIDDLE OCCIPITAL GYRUS; MIDDLE TEMPORAL GYRUS; NEURAL ACTIVATION; NUCLEAR MAGNETIC RESONANCE SCANNER; POSTCENTRAL GYRUS; PRECUNEUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PROBLEM SOLVING; RESPONSE TIME; SELF REPORT; SHORT TERM MEMORY; STROOP TEST; SUPERIOR TEMPORAL GYRUS; TASK PERFORMANCE; THALAMUS; WORKING MEMORY; ADJUVANT CHEMOTHERAPY; BLOOD; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; BREAST NEOPLASMS; COGNITION DISORDERS; DIAGNOSTIC IMAGING; DRUG EFFECTS; INHIBITION (PSYCHOLOGY); MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; REACTION TIME; SURVIVOR; TREATMENT OUTCOME;

ANTINEOPLASTIC AGENTS; BRAIN; BRAIN MAPPING; BREAST NEOPLASMS; CEREBROVASCULAR CIRCULATION; CHEMOTHERAPY, ADJUVANT; COGNITION DISORDERS; EXECUTIVE FUNCTION; FEMALE; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MIDDLE AGED; OXYGEN; REACTION TIME; STROOP TEST; SURVIVORS; TREATMENT OUTCOME;

EID: 84944910108     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-015-9464-7     Document Type: Article

References (57)

1. Abraham, J., Haut, M. W., Moran, M. T., Filburn, S., Lemiuex, S., & Kuwabara, H. (2008). Adjuvant chemotherapy for breast cancer: effects on cerebral white matter seen in diffusion tensor imaging. Clinical Breast Cancer, 8(1), 88–91. doi:10.3816/CBC.2008.n.007.
2. Ahles, T. A., Saykin, A. J., Furstenberg, C. T., Cole, B., Mott, L. A., Skalla, K., & Whedon, M. B. (2002). Neuropsychologic impact of standard-dose systemic chemotherapy in long-term survivors of breast cancer and lymphoma. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology, 20(2), 485–93. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11786578.
3. Alvarez, J. A., & Emory, E. (2006). Executive function and the frontal lobes: a meta-analytic review. Neuropsychology Review, 16(1), 17–42. doi:10.1007/s11065-006-9002-x.
4. Aron, A. R. (2007). The neural basis of inhibition in cognitive control. The Neuroscientist, 13(3), 214–28. doi:10.1177/1073858407299288.
5. Bench, C. J., Frith, C. D., Grasby, P. M., Friston, K. J., Paulesu, E., Frackowiak, R. S. J., & Dolan, R. J. (1993). Investigations of the functional anatomy of attention using the Stroop test. Neuropsychologia, 31(9), 907–922.
6. Blasi, G., Goldberg, T. E., Weickert, T., Das, S., Kohn, P., Zoltick, B., Bertolino, A., et al. (2006). Brain regions underlying response inhibition and interference monitoring and suppression. The European Journal of Neuroscience, 23(6), 1658–64. doi:10.1111/j.1460-9568.2006.04680.x.
7. Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108(3), 624–652. doi:10.1037//0033-295X.I08.3.624.
8. Brezden, B. C. B., Phillips, K., Abdolell, M., Bunston, T., & Tannock, I. F. (2000). Cognitive function in breast cancer patients receiving adjuvant chemotherapy. Journal of Clinical Oncology, 18, 2695–2701.
9. Burock, M. A., Buckner, R. L., Woldorff, M. G., Rosen, B. R., & Dale, A. M. (1998). Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI. Neuroreport, 9(16), 3735–3739.
10. Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Cingulate Cortex, 4(6), 215–222.
11. Campbell, K. L., van Patten, C. L., Neil, S. E., Kirkham, A. A., Gotay, C. C., Gelmon, K. A., et al. (2012a). Feasibility of a lifestyle intervention on body weight and serum biomarkers in breast cancer survivors with overweight and obesity. Journal of the Academy of Nutrition and Dietetics, 112(4), 559–567.
12. Campbell, K. L., Pusic, A. L., Zucker, D. S., McNeely, M. L., Binkley, J. M., Cheville, A. L., et al. (2012b). A prospective model of care for breast cancer rehabilitation: function. Cancer, 118, 2300–2311.
13. Campbell, K. L., Kam, J. W. Y., Boyd, L. A., Handy, T. C., Lim, H., Hayden, S., Hsu, L., et al. (2014). Effect of exercise on cancer-associated cognitive dysfunction: a proof-of-concept randomized controlled trial. Annual Meeting of the American Society of Clinical Oncology.
14. Carter, C. S., Braver, T. S., Barch, D. M., Botvinick, M. M., Noll, D., Cohen, J. D., Botvinick, M. M., et al. (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science, 280(5364), 747–749.
15. Chen, X., Li, J., Ren, J., Hu, X., Zhu, C., Tian, Y., Hu, P., et al. (2014). Selective impairment of attention networks in breast cancer patients receiving chemotherapy treatment. Psycho-Oncology, 10, 10. doi:10.1002/pon.
16. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.
17. de Ruiter, M. B., & Schagen, S. B. (2013). Functional MRI studies in non-CNS cancers. Brain Imaging and Behavior, 7(4), 388–408. doi:10.1007/s11682-013-9249-9.
18. de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., van Dam Nederveen, F. S. A. M., & Boven, A. J. (2011). Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Human Brain Mapping, 32(8), 1206–19. doi:10.1002/hbm.21102.
19. de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., Caan, M., Douaud, G., Lavini, C., et al. (2012). Late effects of high-dose adjuvant chemotherapy on white and gray matter in breast cancer survivors: converging results from multimodal magnetic resonance imaging. Human Brain Mapping, 33(12), 2971–83. doi:10.1002/hbm.21422.
20. Deprez, S., Amant, F., Smeets, A., Peeters, R., Leemans, A., Van Hecke, W., et al. (2012). Longitudinal assessment of chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning. Journal of Clinical Oncology, 30(3), 274–281.
21. Deprez, S., Vandenbulcke, M., Peeters, R., Emsell, L., Smeets, A., Christiaens, M., et al. (2014). Longitudinal assessment of chemotherapy-induced alterations in brain activation during multitasking and its relation with cognitive complaints. Journal of Clinical Oncology, 32(19), 2031–8.
22. Erickson, K. I., Prakash, R. S., Kim, J. S., Sutton, B. P., Colcombe, S. J., & Kramer, A. F. (2009). Top-down attentional control in spatially coincident stimuli enhances activity in both task-relevant and task-irrelevant regions of cortex. Behavioural Brain Research, 197(1), 186–97. doi:10.1016/j.bbr.2008.08.028.
23. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance in Medicine, 33, 636–647.
24. Ganz, P. A., Kwan, L., Castellon, S. A., Oppenheim, A., Bower, J. E., Silverman, D. H. S., & Cole, S. W. (2013). Cognitive complaints after breast cancer treatments: examining the relationship with neuropsychological test performance. Journal of the National Cancer Institute, 105(11), 791–801. doi:10.1093/jnci/djt073.
25. Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86, 141–155.
26. Inagaki, M., Yoshikawa, E., Matsuoka, Y., Sugawara, Y., Nakano, T., Akechi, T., Wada, N., et al. (2007). Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy. Cancer, 109(1), 146–56. doi:10.1002/cncr.22368.
27. Jim, H. S. L., Phillips, K. M., Chait, S., Faul, L. A., Popa, M. A., Lee, Y.-H., & Hussin, M. G. (2012). Meta-analysis of cognitive functioning in breast cancer survivors previously treated with standard-dose chemotherapy. Journal of Clinical Oncology, 30(29), 3578–87. doi:10.1200/JCO.2011.39.5640.
28. Kam, J. W. Y., Brenner, C. A., Handy, T. C., Boyd, L. A., Liu-Ambrose, T., Lim, H. J., Hayden, S., et al. (2015). Sustained attention abnormalities in breast cancer survivors with cognitive deficits post chemotherapy: an electrophysiological study. Clinical Neurophysiology. doi:10.1016/j.clinph.2015.03.007.
29. Kesler, S. R., Bennett, F. C., Mahaffey, M. L., & Spiegel, D. (2009). Regional brain activation during verbal declarative memory in metastatic breast cancer. Clinical Cancer Research, 15(21), 6665–6673. doi:10.1158/1078-0432.CCR-09-1227.Regional.
30. Kesler, S. R., Kent, J. S., & Hara, R. O. (2011). Prefrontal cortex and executive function impairments in primary breast cancer. Archives of Neurology, 68(11), 1447–1453.
31. Kesler, S., Janelsins, M., Koovakkattu, D., Palesh, O., Mustian, K., Morrow, G., & Dhabhar, F. S. (2013). Reduced hippocampal volume and verbal memory performance associated with interleukin-6 and tumor necrosis factor-alpha levels in chemotherapy-treated breast cancer survivors. Brain, Behavior, and Immunity, 30(Suppl), S109–16. doi:10.1016/j.bbi.2012.05.017.
32. Koppelmans, V., de Ruiter, M. B., van der Lijn, F., Boogerd, W., Seynaeve, C., van der Lugt, A., Vrooman, H., et al. (2012). Global and focal brain volume in long-term breast cancer survivors exposed to adjuvant chemotherapy. Breast Cancer Research and Treatment, 132(3), 1099–106. doi:10.1007/s10549-011-1888-1.
33. Koppelmans, V., de Groot, M., de Ruiter, M. B., Boogerd, W., Seynaeve, C., Vernooij, M. J., et al. (2014). Global and focal white matter integrity in breast cancer survivors 20 years after adjuvant chemotherapy. Human Brain Mapping, 35(3), 889–899.
34. Leung, H., Skudlarski, P., Gatenby, J. C., Peterson, B. S., & Gore, J. C. (2000). An event-related functional MRI study of the Stroop color word interference task. Cerebral Cortex, 10, 552–560.
35. Lindner, O. C., Phillips, B., McCabe, M. G., Maves, A. Wearden, A., Varese, F., & Talmi D. (2014). A meta-analysis of cognitive impairment following adult cancer chemotherapy. Neuropsychology.
36. López Zunini, R. A., Scherling, C., Wallis, N., Collins, B., MacKenzie, J., Bielajew, C., & Smith, A. M. (2013). Differences in verbal memory retrieval in breast cancer chemotherapy patients compared to healthy controls: a prospective fMRI study. Brain Imaging and Behavior, 7(4), 460–77. doi:10.1007/s11682-012-9213-0.
37. MacDonald, A. W., Cohen, J. D., Stenger, V. A., & Cameron, S. (2000). Dissociating the role of dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835–1838.
38. McDonald, B. C., & Saykin, A. J. (2013). Alterations in brain structure related to breast cancer and its treatment: chemotherapy and other considerations. Brain Imaging and Behavior, 7(4), 374–87. doi:10.1007/s11682-013-9256-x.
39. McDonald, B. C., Conroy, S. K., Ahles, T. A., West, J. D., & Saykin, A. J. (2010). Gray matter reduction associated with systemic chemotherapy for breast cancer: a prospective MRI study. Breast Cancer Research and Treatment, 123(3), 819–28. doi:10.1007/s10549-010-1088-4.
40. McDonald, B. C., Conroy, S. K., Ahles, T. A., West, J. D., & Saykin, A. J. (2012). Alterations in brain activations during working memory processing associated with breast cancer and treatment: a prospective functional magnetic resonance imaging study. Journal of Clinical Oncology, 30(20), 2500–2508.
41. McDonald, B. C., Conroy, S. K., Smith, D. J., West, J. D., & Saykin, A. J. (2013). Frontal gray matter reduction after breast cancer chemotherapy and association with executive symptoms: a replication and extension study. Brain, Behavior, and Immunity, 30(Suppl), S117–25. doi:10.1016/j.bbi.2012.05.007.
42. McNeely, M. L., Campbell, K. L., Rowe, B. H., Klassen, T. P., Mackey, J. R., & Courneya, K. S. (2006). Effects of exercise on breast cancer patients and survivors: a systematic review and meta-analysis. Canadian Medical Association Journal, 175(1), 34–41.
43. Milham, M. P., Banich, M. T., Webb, A., Barad, V., Cohen, N. J., Wszalek, T., & Kramer, A. F. (2001). The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. Cognitive Brain Research, 12, 467–473.
44. 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. doi:10.1006/cogp.1999.0734.
45. Morooka, T., Ogino, T., Takeuchi, A., Hanafusa, K., Oka, M., & Ohtsuka, Y. (2012). Relationships between the color-word matching Stroop task and the go/nogo task: toward multifaceted assessment of attention and inhibition abilities of children. Acta Medica Okayama, 66(5), 377–386.
46. Mostofsky, S. H., & Simmonds, D. J. (2008). Response inhibition and response selection: two sides of the same coin. Journal of Cognitive Neuroscience, 20(5), 751–761.
47. Prakash, R. S., Voss, M. W., Erickson, K. I., Lewis, J. M., Chaddock, L., Malkowski, E., Alves, H., et al. (2011). Cardiorespiratory fitness and attentional control in the aging brain. Frontiers in Human Neuroscience, 4(January), 229. doi:10.3389/fnhum.2010.00229.
48. Reuter-Lorenz, P. A., & Cimprich, B. (2013). Cognitive function and breast cancer: promise and potential insights from functional brain imaging. Breast Cancer Research and Treatment, 137(1), 33–43. doi:10.1007/s10549-012-2266-3.
49. Robinson, J. L., Laird, A. R., Glahn, D. C., Blangero, J., Sanghera, M. K., Pessoa, L., et al. (2012). The functional connectivity of the human caudate: an application of meta-analytic connectivity modeling with behavioral filtering. NeuroImage, 60, 117–129.
50. Schagen, S. B., van Dam, F. S., Muller, M. J., Boogerd, W., Lindeboom, J., & Bruning, P. F. (1999). Cognitive deficits after postoperative adjuvant chemotherapy for breast carcinoma. Cancer, 85(3), 640–50. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10091737.
51. Scherling, C., Collins, B., Mackenzie, J., Bielajew, C., & Smith, A. (2012). Prechemotherapy differences in response inhibition in breast cancer patients compared to controls: a functional magnetic resonance imaging study. Journal of Clinical and Experimental Neuropsychology, 34(5), 543–60. doi:10.1080/13803395.2012.666227.
52. Schmahmann, J. D., Doyon, J., Mcdonald, D., Holmes, C., Lavoie, K., Hurwitz, A. S., Kabani, N., et al. (1999). Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. NeuroImage, 10, 233–260.
53. Smallwood, J., Brown, K., Baird, B., & Schooler, J. W. (2012). Cooperation between the default mode network and the frontal-parietal network in the production of an internal train of thought. Brain Research, 1428, 60–70. doi:10.1016/j.brainres.2011.03.072.
54. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. Proceedings of the National Academy of Sciences of the United States of America (Vol. 106). New York, NY: Thieme. doi:10.1073/pnas.0900234106.
55. Vaughan, L., & Giovanello, K. (2010). Executive function in daily life: age-related influences of executive processes on instrumental activities of daily living. Psychology of Aging, 25, 343–355.
56. Vearncombe, K. J., Rolfe, M., Wright, M., Pachana, N. A., Andrew, B., & Beadle, G. (2009). Predictors of cognitive decline after chemotherapy in breast cancer patients. Journal of International Neuropsychological Society, 15(6), 951–962.
57. Vendrell, P., Junque, C., Pujol, J., Jurado, M. A., Molet, J., & Grafmanll, J. (1995). The role of prefrontal regions in the Stroop task. Neuropsychologia, 33(3), 341–352.