Abstract
It has been hypothesized that breast cancer and its chemotherapy can impart functional neural changes via an overlap with biological mechanisms associated with aging. Here we used fMRI to assess whether changes in neural activity accompanying visual episodic memory encoding and retrieval suggest altered activations according to patterns seen in functional imaging of cognitive aging. In a prospective longitudinal design, breast cancer patients (n = 13) were scanned during memory encoding and retrieval before and after chemotherapy treatment, and compared to healthy-age matched controls (n = 13). Our results indicate that despite equivalent behavioral performance, encoding and retrieval resulted in increased activation of prefrontal regions for the breast cancer group compared to controls for both before and after chemotherapy treatment. This was accompanied by decreased activity in posterior brain regions after chemotherapy, particularly those involved in visual processing, for the breast cancer group compared to controls. These findings are discussed as evidence for a possible anterior shift in neural processing to compensate for deficiencies in posterior brain regions, consistent with an accelerated aging account. Cancer and chemotherapy can impact brain regions underlying episodic memory, leading to additional recruitment of control regions, which may be linked to mechanisms related to aging.
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References
Ahles, T. A., & Root, J. C. (2018). Cognitive effects of Cancer and Cancer treatments. Annual Review of Clinical Psychology, 14(8), 425–451. https://doi.org/10.1146/annurev-clinpsy-050817-084903.
Ahles, T. A., Root, J. C., & Ryan, E. L. (2012). Cancer- and cancer treatment-associated cognitive change: An update on the state of the science. Journal of Clinical Oncology, 30(30), 3675–3686. https://doi.org/10.1200/JCO.2012.43.0116.
Al-Tweigeri, T., Nabholtz, J. M., & Mackey, J. R. (1996). Ocular toxicity and cancer chemotherapy. Cancer, 78(7), 1359–1373. https://doi.org/10.1002/(SICI)1097-0142(19961001)78:7<1359::AID-CNCR1>3.0.CO;2-G.
Anderson, N. D., Iidaka, T., Cabeza, R., Kapur, S., McIntosh, A. R., & Craik, F. I. (2000). The effects of divided attention on encoding- and retrieval-related brain activity: A PET study of younger and older adults. Journal of Cognitive Neuroscience, 12(5), 775–792. https://doi.org/10.1162/089892900562598.
Anstey, K. J., Butterworth, P., Borzycki, M., & Andrews, S. (2006). Between- and within-individual effects of visual contrast sensitivity on perceptual matching, processing speed, and associative memory in older adults. Gerontology, 52(2), 124–130. https://doi.org/10.1159/000090958.
Badiola, I., Santaolalla, F., Garcia-Gallastegui, P., Ana, S. R., Unda, F., & Ibarretxe, G. (2015). Biomolecular bases of the senescence process and cancer. A new approach to oncological treatment linked to ageing. Ageing Research Reviews, 23(Pt B), 125–138. https://doi.org/10.1016/j.arr.2015.03.004.
Blumenfeld, R. S., & Ranganath, C. (2007). Prefrontal cortex and long-term memory encoding: An integrative review of findings from neuropsychology and neuroimaging. Neuroscientist, 13(3), 280–291. https://doi.org/10.1177/1073858407299290.
Botvinick, M. M., Cohen, J. D., & Carter, C. S. (2004). Conflict monitoring and anterior cingulate cortex: An update. Trends in Cognitive Sciences, 8(12), 539–546. https://doi.org/10.1016/j.tics.2004.10.003.
Buckner, R. L., Koutstaal, W., Schacter, D. L., Wagner, A. D., & Rosen, B. R. (1998). Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success. NeuroImage, 7(3), 151–162. https://doi.org/10.1006/nimg.1998.0327.
Bunge, S. A., Burrows, B., & Wagner, A. D. (2004). Prefrontal and hippocampal contributions to visual associative recognition: Interactions between cognitive control and episodic retrieval. Brain and Cognition, 56(2 SPEC. ISS.), 141–152. https://doi.org/10.1016/j.bandc.2003.08.001
Cabeza, R., & Dennis, N. A. (2012). Frontal lobes and aging. In Principles of Frontal Lobe Function (pp. 628–652). https://doi.org/10.1093/acprof:oso/9780195134971.001.0001.
Cabeza, R., Grady, C. L., Nyberg, L., McIntosh, A. R., Tulving, E., Kapur, S., et al. (1997). Age-related differences in neural activity during memory encoding and retrieval: A positron emission tomography study. The Journal of Neuroscience, 17(1), 391–400.
Cabeza, R., Anderson, N. D., Locantore, J. K., & McIntosh, A. R. (2002). Aging gracefully: Compensatory brain activity in high-performing older adults. NeuroImage, 17(3), 1394–1402. https://doi.org/10.1006/nimg.2002.1280.
Cabeza, R., Daselaar, S. M., Dolcos, F., Prince, S. E., Budde, M., & Nyberg, L. (2004). Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cerebral Cortex, 14(4), 364–375.
Chen, M. L., Miaskowski, C., Liu, L. N., & Chen, S. C. (2012). Changes in perceived attentional function in women following breast cancer surgery. Breast Cancer Research and Treatment, 131(2), 599–606. https://doi.org/10.1007/s10549-011-1760-3.
Chun, M. M., & Johnson, M. K. (2011). Memory: Enduring traces of perceptual and reflective attention. Neuron, 72(4), 520–535. https://doi.org/10.1016/j.neuron.2011.10.026.
Cimprich, B., Reuter-Lorenz, P., Nelson, J., Clark, P. M., Therrien, B., Normolle, D., et al. (2010). Prechemotherapy alterations in brain function in women with breast cancer. Journal of Clinical and Experimental Neuropsychology, 32(3), 324–331. https://doi.org/10.1080/13803390903032537.
Cohen, J. D., Botvinick, M., & Carter, C. S. (2000). Anterior cingulate and prefrontal cortex: who’s in control? Nature Neuroscience, 3(5), 421–423. https://doi.org/10.1038/74783.
Conroy, S. K., McDonald, B. C., Ahles, T. A., West, J. D., & Saykin, A. J. (2013a). Chemotherapy-induced amenorrhea: A prospective study of brain activation changes and neurocognitive correlates. Brain Imaging and Behavior, 7(4), 491–500. https://doi.org/10.1007/s11682-013-9240-5.
Conroy, S. K., McDonald, B. C., Smith, D. J., Moser, L. R., West, J. D., Kamendulis, L. M., et al. (2013b). Alterations in brain structure and function in breast cancer survivors: Effect of post-chemotherapy interval and relation to oxidative DNA damage. Breast Cancer Research and Treatment, 137(2), 493–502. https://doi.org/10.1007/s10549-012-2385-x.
Craik, F. I. M. (2002). Levels of processing: Past, present... And future? Memory, 10(5–6), 305–318. https://doi.org/10.1080/09658210244000135.
Craik, F. I. M., & Lockhart, R. S. (1972). Levels of processing: A framework for memory research. Journal of Verbal Learning and Verbal Behavior, 11(6), 671–684. https://doi.org/10.1016/S0022-5371(72)80001-X.
Daselaar, S. M., Veltman, D. J., Rombouts, S. A. R. B., Raaijmakers, J. G. W., & Jonker, C. (2003). Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. Brain: A Journal of Neurology, 126(Pt 1), 43–56. https://doi.org/10.1093/brain/awg005.
Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S., & Cabeza, R. (2008). Que PASA? The posterior-anterior shift in aging. Cerebral Cortex, 18(5), 1201–1209. https://doi.org/10.1093/cercor/bhm155.
de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., van Dam, F. S. A. M., Nederveen, A. J., et al. (2011). Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Human Brain Mapping, 32(8), 1206–1219. https://doi.org/10.1002/hbm.21102.
Dennis, N. A., Hayes, S. M., Prince, S. E., Madden, D. J., Huettel, S. A., & Cabeza, R. (2008). Effects of aging on the neural correlates of successful item and source memory encoding. Journal of Experimental Psychology. Learning, Memory, and Cognition, 34(4), 791–808. https://doi.org/10.1037/0278-7393.34.4.791.
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. https://doi.org/10.1200/JCO.2011.36.8571.
Deprez, S., Vandenbulcke, M., Peeters, R., Emsell, L., Smeets, A., Christiaens, M. R., 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), 2031–2038. https://doi.org/10.1200/JCO.2013.53.6219.
Downie, F. P., Mar Fan, H. G., Houédé-Tchen, N., Yi, Q., & Tannock, I. F. (2006). Cognitive function, fatigue, and menopausal symptoms in breast cancer patients receiving adjuvant chemotherapy: Evaluation with patient interview after formal assessment. Psycho-Oncology, 15(10), 921–930. https://doi.org/10.1002/pon.1035.
Eisner, A., & Luoh, S. W. (2011). Breast cancer medications and vision: Effects of treatments for early-stage disease. Current Eye Research, 36(10), 867–885. https://doi.org/10.3109/02713683.2011.594202.
Ferguson, R. J., Mcdonald, B. C., Saykin, A. J., & Ahles, T. A. (2007). Brain structure and function differences in monozygotic twins: Possible effects of breast Cancer therapy. Journal of Clinical Oncology, 25(25), 3866–3870. https://doi.org/10.1200/JCO.2007.10.8639 Brain.
Frank, L. R., Buxton, R. B., Wong, E. C. (2001). Estimation of respiration-induced noise fluctuations from undersampled multislice fMRI data. Magnetic Resonance in Medicine, 45(4), 635–644. https://doi.org/10.1002/mrm.1086.
Frank, J. S., Vance, D. E., Jukkala, A., & Meneses, K. M. (2014). Attention and memory deficits in breast cancer survivors: Implications for nursing practice and research. Journal of Neuroscience Nursing, 46(5), 274–284. https://doi.org/10.1097/JNN.0000000000000078.
Grady, C. L., Maisog, J. M., Horwitz, B., Ungerleider, L. G., Mentis, M. J., Salerno, J. A., et al. (1994). Age-related changes in cortical blood flow activation during visual processing of faces and location. The Journal of Neuroscience, 14(3 Pt 2), 1450–1462. https://doi.org/10.1080/09541440042000304.
Grady, C. L., McIntosh, A. R., Rajah, M. N., Beig, S., & Craik, F. I. M. (1999). The effects of age on the neural correlates of episodic encoding. Cerebral Cortex, 9(8), 805–814. https://doi.org/10.1093/Cercor/9.8.805.
Grady, C. L., Bernstein, L. J., Beig, S., & Siegenthaler, A. L. (2002). The effects of encoding task on age-related differences in the functional neuroanatomy of face memory. Psychology and Aging, 17(1), 7–23.
Gutchess, A. H., Welsh, R. C., Hedden, T., Bangert, A., Minear, M., Liu, L. L., & Park, D. C. (2005). Aging and the neural correlates of successful picture encoding: Frontal activations compensate for decreased medial-temporal activity. Journal of Cognitive Neuroscience, 17(1), 84–96. https://doi.org/10.1162/0898929052880048.
Gutchess, A. H., Hebrank, A., Sutton, B. P., Leshikar, E., Chee, M. W. L., Tan, J. C., et al. (2007). Contextual interference in recognition memory with age. NeuroImage, 35(3), 1338–1347. https://doi.org/10.1016/j.neuroimage.2007.01.043.
Jacoby, L. L. (1991). A process dissociation framework: Separating automatic from intentional uses of memory. Journal of Memory and Language, 30, 513–541. https://doi.org/10.1016/0749-596X(91)90025-F.
Jim, H. S. L., Phillips, K. M., Chait, S., Faul, L. A., Popa, M. A., Lee, Y.-H., et al. (2012). Meta-analysis of cognitive functioning in breast Cancer survivors previously treated with standard-dose chemotherapy. Journal of Clinical Oncology, 30(29), 3578–3587. https://doi.org/10.1200/JCO.2011.39.5640.
Kam, J. W. Y., Brenner, C. A., Handy, T. C., Boyd, L. A., Liu-Ambrose, T., Lim, H. J., et al. (2015). Sustained attention abnormalities in breast cancer survivors with cognitive deficits post chemotherapy: An electrophysiological study. Clinical Neurophysiology, 127, 369–378. https://doi.org/10.1016/j.clinph.2015.03.007.
Kapur, S., Craik, F. I., Tulving, E., Wilson, A. A., Houle, S., & Brown, G. M. (1994). Neuroanatomical correlates of encoding in episodic memory: Levels of processing effect. Proceedings of the National Academy of Sciences of the United States of America, 91(6), 2008–2011. https://doi.org/10.1073/pnas.91.6.2008.
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. https://doi.org/10.1158/1078-0432.CCR-09-1227.
Kohli, S., Griggs, J. J., Roscoe, J. a., Jean-Pierre, P., Bole, C., Mustian, K. M., et al. (2007). Self-reported cognitive impairment in patients with Cancer. Journal of Oncology Practice, 3(2), 54–59. https://doi.org/10.1200/JOP.0722001.
Leshikar, E. D., Gutchess, A. H., Hebrank, A. C., Sutton, B. P., & Park, D. C. (2010). The impact of increased relational encoding demands on frontal and hippocampal function in older adults. Cortex, 46(4), 507–521. https://doi.org/10.1016/j.cortex.2009.07.011.
Leshikar, E. D., Duarte, A., & Hertzog, C. (2012). Task-selective memory effects for successfully implemented encoding strategies. PLoS One, 7(5), e38160. https://doi.org/10.1371/journal.pone.0038160.
Levy, B. J., & Anderson, M. C. (2002). Inhibitory process and the control of memory retrieval. Trends in Cognitive Sciences, 6(7), 299–305.
Li, S. C., Lindenberger, U., & Frensch, P. A. (2000). Unifying cognitive aging: From neuromodulation to representation to cognition. Neurocomputing, 32–33(November 2016), 879–890. https://doi.org/10.1016/S0925-2312(00)00256-3.
Li, S. C., Lindenberger, U., & Sikström, S. (2001). Aging cognition: From neuromodulation to representation. Trends in Cognitive Sciences, 5(11), 479–486. https://doi.org/10.1016/S1364-6613(00)01769-1.
Logan, J. M., Sanders, A. L., Snyder, A. Z., Morris, J. C., & Buckner, R. L. (2002). Under-recruitment and nonselective recruitment: Dissociable neural mechanisms associated with aging. Neuron, 33(5), 827–840. https://doi.org/10.1016/S0896-6273(02)00612-8.
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), 460–477. https://doi.org/10.1007/s11682-012-9213-0.
Madden, D. J., Gottlob, L. R., Denny, L. L., Turkington, T. G., Provenzale, J. M., Hawk, T. C., & Coleman, R. E. (1999). Aging and recognition memory: Changes in regional cerebral blood flow associated with components of reaction time distributions. Journal of Cognitive Neuroscience, 11(5), 511–520. https://doi.org/10.1162/089892999563571.
Mandelblatt, J. S., Hurria, A., McDonald, B. C., Saykin, A. J., Stern, R. A., VanMeter, J. W., et al. (2013). Cognitive effects of Cancer and its treatments at the intersection of aging: What do we know; what do we need to know? Seminars in Oncology, 40(6), 709–725. https://doi.org/10.1053/j.seminoncol.2013.09.006.
Mandzia, J. L., Black, S. E., McAndrews, M. P., Grady, C., & Graham, S. (2004). fMRI differences in encoding and retrieval of pictures due to encoding strategy in the elderly. Human Brain Mapping, 21(1), 1–14. https://doi.org/10.1002/hbm.10140.
McDonald, B. C., Conroy, S. K., Ahles, T. A., West, J. D., & Saykin, A. J. (2012). Alterations in brain activation 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. https://doi.org/10.1200/JCO.2011.38.5674.
Menning, S., de Ruiter, M. B., Veltman, D. J., Boogerd, W., Oldenburg, H. S. A., Reneman, L., & Schagen, S. B. (2017). Changes in brain activation in breast cancer patients depend on cognitive domain and treatment type. PLoS One, 12(3), e0171724. https://doi.org/10.1371/journal.pone.0171724.
Morcom, A. M., Good, C. D., Frackowiak, R. S. J., & Rugg, M. D. (2003). Age effects on the neural correlates of successful memory encoding. Brain, 126(1), 213–229. https://doi.org/10.1093/brain/awg020.
Nyberg, L. (2010). Levels of processing: A view from functional brain imaging. Memory, 10(5–6), 345–348. https://doi.org/10.1080/09658210244000171.
Otten, L. J., Henson, R. N., & Rugg, M. D. (2001). Depth of processing effects on neural correlates of memory encoding: Relationship between findings from across- and within-task comparisons. Brain, 124(Pt 2), 399–412.
Pan, H., Epstein, J., Silbersweig, D. A., & Stern, E. (2011). New and emerging imaging techniques for mapping brain circuitry. Brain Research Reviews, 67(1–2), 226–251. https://doi.org/10.1016/j.brainresrev.2011.02.004.
Park, D. C., Polk, T. A., Mikels, J. A., Taylor, S. F., & Marshuetz, C. (2001). Cerebral aging: Integration of brain and behavioral models of cognitive function. Dialogues in Clinical Neuroscience, 3(3), 151–165. https://doi.org/10.1016/0025-5416(76)90216-0.
Perez, D. L., Pan, H., Weisholtz, D. S., Root, J. C., Tuescher, O., Fischer, D. B., et al. (2015). Altered threat and safety neural processing linked to persecutory delusions in schizophrenia: A two-task fMRI study. Psychiatry Research: Neuroimaging, 233(3), 352–366. https://doi.org/10.1016/j.pscychresns.2015.06.002.
Preston, A. R., & Eichenbaum, H. (2013). Interplay of hippocampus and prefrontal cortex in memory. Current Biology, 23(17), R764–R773. https://doi.org/10.1016/j.cub.2013.05.041.
Prince, S. E., Dennis, N. A., & Cabeza, R. (2009). Encoding and retrieving faces and places: Distinguishing process- and stimulus-specific differences in brain activity. Neuropsychologia, 47(11), 2282–2289. https://doi.org/10.1016/j.neuropsychologia.2009.01.021.
Raffa, R. B., & Tallarida, R. J. (2010). Effects on the visual system might contribute to some of the cognitive deficits of cancer chemotherapy-induced ‘chemo-fog. Journal of Clinical Pharmacy and Therapeutics, 35(3), 249–255. https://doi.org/10.1111/j.1365-2710.2009.01086.x.
Reuter-Lorenz, P. A., & Cappell, K. A. (2008). Neurocognitive ageing and the compensation hypothesis. Current Directions in Psychological Science, 17, 177–182.
Rorden, C., & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioural Neurology, 12(4), 191–200. https://doi.org/10.1155/2000/421719.
Sanoff, H. K., Deal, A. M., Krishnamurthy, J., Torrice, C., Dillon, P., Sorrentino, J., et al. (2014). Effect of cytotoxic chemotherapy on markers of molecular age in patients with breast cancer. Journal of the National Cancer Institute, 106(4), 1–8. https://doi.org/10.1093/jnci/dju057.
Sato, C., Sekiguchi, A., Kawai, M., Kotozaki, Y., Nouchi, R., Tada, H., et al. (2015). Postoperative structural brain changes and cognitive dysfunction in patients with breast cancer. PLoS One, 10(11), 1–16. https://doi.org/10.1371/journal.pone.0140655.
Scherling, C., Collins, B., Mackenzie, J., Bielajew, C., & Smith, A. (2011). Pre-chemotherapy differences in visuospatial working memory in breast cancer patients compared to controls: An FMRI study. Frontiers in Human Neuroscience, 5(November), 122. https://doi.org/10.3389/fnhum.2011.00122.
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), 543–560. https://doi.org/10.1080/13803395.2012.666227.
Shiffrin, R. M., & Schneider, W. (1984). Automatic and controlled processing revisited. Psychological Review, 91(2), 269–276. https://doi.org/10.1037/0033-295X.91.2.269.
Silverman, D. H. S., Dy, C. J., Castellon, S. A., Lai, J., Pio, B. S., Abraham, L., et al. (2007). Altered frontocortical, cerebellar, and basal ganglia activity in adjuvant-treated breast cancer survivors 5-10 years after chemotherapy. Breast Cancer Research and Treatment, 103(3), 303–311. https://doi.org/10.1007/s10549-006-9380-z.
Skeel, R. L., Schutte, C., van Voorst, W., & Nagra, A. (2006). The relationship between visual contrast sensitivity and neuropsychological performance in a healthy elderly sample. Journal of Clinical and Experimental Neuropsychology, 28(5), 696–705. https://doi.org/10.1080/13803390590954173.
Sperling, R. A., Bates, J. F., Chua, E. F., Cocchiarella, A. J., Rentz, D. M., Rosen, B. R., et al. (2003). fMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 74(1), 44–50.
Stouten-Kemperman, M. M., de Ruiter, M. B., Koppelmans, V., Boogerd, W., Reneman, L., & Schagen, S. B. (2014). Neurotoxicity in breast cancer survivors ≥10 years post-treatment is dependent on treatment type. Brain Imaging and Behavior, (2015), 275–284. https://doi.org/10.1007/s11682-014-9305-0.
Tulving, E., Kapur, S., Craik, F. I., Moscovitch, M., & Houle, S. (1994). Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission tomography findings. Proceedings of the National Academy of Sciences of the United States of America, 91(6), 2016–2020.
Weisholtz, D. S., Root, J. C., Butler, T., Tüscher, O., Epstein, J., Pan, H., et al. (2015). Beyond the amygdala: Linguistic threat modulates peri-sylvian semantic access cortices. Brain and Language, 151(3), 12–22. https://doi.org/10.1016/j.bandl.2015.10.004.
Wood, J., Chaparro, A., Anstey, K., Lacherez, P., Chidgey, A., Eisemann, J., et al. (2010). Simulated visual impairment leads to cognitive slowing in older adults. Optometry and Vision Science, 87(12), 1037–1043. https://doi.org/10.1097/OPX.0b013e3181fe64d7.
Worsley, K. J., Liao, C. H., Aston, J., Petre, V., Duncan, G. H., Morales, F., & Evans, A. C. (2002). A general statistical analysis for fMRI data. NeuroImage, 15(1), 1–15. https://doi.org/10.1006/nimg.2001.0933.
Yao, C., Rich, J. B., Tannock, I. F., Seruga, B., Tirona, K., & Bernstein, L. J. (2016). Pretreatment differences in Intraindividual variability in reaction time between women diagnosed with breast Cancer and healthy controls. Journal of the International Neuropsychological Society, 22(05), 530–539. https://doi.org/10.1017/S1355617716000126.
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TAA and SDP were supported by the Starr Cancer Consortium (protocol #1-A17) and Amgen, Inc. DP would like to acknowledge the NIH/NCI Cancer Center Support Grant P30 CA008748 and the NCI award number T32 CA009461 under which authorship for this work was supported. The content is solely responsible of the authors and does not necessarily represent the official views of the National Institutes of Health.
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Denise Pergolizzi, James C. Root, Hong Pan, David Silbersweig, Emily Stern, Steven D. Passik and Tim A. Ahles declare that they have no conflict of interest.
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Pergolizzi, D., Root, J.C., Pan, H. et al. Episodic memory for visual scenes suggests compensatory brain activity in breast cancer patients: a prospective longitudinal fMRI study. Brain Imaging and Behavior 13, 1674–1688 (2019). https://doi.org/10.1007/s11682-019-00038-2
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DOI: https://doi.org/10.1007/s11682-019-00038-2