Pre-chemotherapy differences in visuospatial working memory in breast cancer patients compared to controls: an FMRI study

Carole Scherling, Barbara Collins, Joyce Mackenzie, Catherine Bielajew, Andra Smith, Carole Scherling, Barbara Collins, Joyce Mackenzie, Catherine Bielajew, Andra Smith

Abstract

Introduction: Cognitive deficits are a side-effect of chemotherapy, however pre-treatment research is limited. This study examines neurofunctional differences during working memory between breast cancer (BC) patients and controls, prior to chemotherapy.

Methods: Early stage BC females (23), scanned after surgery but before chemotherapy, were individually matched to non-cancer controls. Participants underwent functional magnetic resonance imaging (fMRI) while performing a Visuospatial N-back task and data was analyzed by multiple group comparisons. fMRI task performance, neuropsychological tests, hospital records, and salivary biomarkers were also collected.

Results: There were no significant group differences on neuropsychological tests, estrogen, or cortisol. Patients made significantly fewer commission errors but had less overall correct responses and were slower than controls during the task. Significant group differences were observed for the fMRI data, yet results depended on the type of analysis. BC patients presented with increased activations during working memory compared to controls in areas such as the inferior frontal gyrus, insula, thalamus, and midbrain. Individual group regressions revealed a reverse relationship between brain activity and commission errors.

Conclusion: This is the first fMRI investigation to reveal neurophysiological differences during visuospatial working memory between BC patients pre-chemotherapy and controls. These results also increase the knowledge about the effects of BC and related factors on the working memory network.

Significance: This highlights the need to better understand the pre-chemotherapy BC patient and the effects of associated confounding variables.

Keywords: breast cancer; chemotherapy; cognitive impairment; functional magnetic resonance imaging; pre-treatment effects; stress; surgery; visuospatial working memory.

Figures

Figure 1
Figure 1
Diurnal cortisol rhythms for breast cancer patients and matched controls.
Figure 2
Figure 2
Significant t-test results for patients > controls for the 2back-0 contrast. 1. No covariate (left frontal operculum, right midbrain); 2. Reaction time as covariate (bilateral thalamus, right superior occipital gyrus); 3. BDI as covariate (right red nucleus).
Figure 3
Figure 3
Significant flexible factorial results for 0-rest and 2back-rest contrasts. (1) Patients > controls 0-rest contrast; (2) patients < controls 0-rest contrast; (3) patients > controls 2back-rest contrast; (4) patients < controls 2back-rest contrast.

References

    1. Abercrombie H. C., Giese-Davis J., Sephton S., Epel E. S., Turner-Cobb J. M., Spiegel D. (2004). Flattened cortisol rhythms in metastatic breast cancer patients. Psychoneuroendocrinology 29, 1082–109210.1016/j.psyneuen.2003.11.003
    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. Clin. Breast Cancer 8, 88–9110.3816/CBC.2008.n.007
    1. Aguirre G. K., Detre J. A., Alsop D. C., D’Esposito M. (1996). The parahippocampus subserves topographical learning in man. Cereb. Cortex 6, 823–82910.1093/cercor/6.6.823
    1. Ahles T. A., Saykin A. J., Furstenberg C. T., Cole B., Mott L. A., Skalla K., Whedon M. B., Bivens S., Mitchell T., Greenberg E. R., Silberbarb P. M. (2002). Neuropsychologic impact of standard-dose systemic chemotherapy in long-term survivors of breast cancer and lymphoma. J. Clin. Oncol. 20, 485–49310.1200/JCO.20.2.485
    1. Ahles T. A., Tope D. M., Furstenberg C., Hann D., Mills L. (1996). Psychologic and neuropsychologic impact of autologous bone marrow transplantation. J. Clin. Oncol. 14, 1457–1462
    1. Al’Absi M., Hugdahl K., Lovallo W. R. (2002). Adrenocortical stress responses and altered working memory performance. Psychophysiology 39, 95–9910.1111/1469-8986.3910095
    1. Alichniewicz K. K., Nebl H., Klünemann H. H., Greenlee M. W. (2010). The neural correlates of visuo-spatial working memory in patients with amnestic mild cognitive impairment. Eur. Psychiatry 25, 765.10.1016/S0924-9338(10)70555-1
    1. Army Individual Test Battery (1944). Manual for Directions and Scoring. Washington, DC: War Department, Adjutant General’s Office
    1. Aron A. R., Behrens T. E., Smith S., Frank M. J., Poldrack R. A. (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J. Neurosci. 27, 3743–375210.1523/JNEUROSCI.0519-07.2007
    1. Backhaus J., Junghanns K., Hohagen F. (2004). Sleep disturbances are correlated with decreased morning awakening salivary cortisol. Psychoneuroendocrinology 29, 1184–119110.1016/j.psyneuen.2004.01.010
    1. Baddeley A. D. (2000). The episodic buffer: a new component of working memory? Trends Cogn. Sci. 4, 417–42310.1016/S1364-6613(00)01538-2
    1. Baddeley A. D., Hitch G. J. (1974). “Working memory,” in Recent Advances in Learning and Motivation, ed. Bower G. A. (New York: Academic Press; ), 47–89
    1. Barch D. M., Braver T. S., Nystrom L. E., Forman S. D., Noll D. C., Cohen J. D. (1997). Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia 35, 1373–138010.1016/S0028-3932(97)00072-9
    1. Baudino B., D’Agata F., Castellano G., Caroppo P., Cauda S., Parente A., Manfredi M., Geda E., Orsi L., Cauda S., Castelli L., Sacco K., Ardito R., Tora R., Bisi G. (2011). Chemotherapy effects on brain glucose metabolism at rest. Nat. Precedings.
    1. Beck A. T., Steer R. A. (1990). Beck Anxiety Inventory Manual. San Antonio: Psychological Corporation
    1. Beck A. T., Steer R. A., Brown G. K. (1996). Beck Depression Inventory-2nd Edn Manual. San Antonio: Psychological Corporation
    1. Behl C. (2002). Oestrogen as a neuroprotective hormone. Nat. Rev. Neurosci. 3, 433–442
    1. Bender C. M., Sereika S. M., Berga S. L., Vogel V. G., Brufksy A. M., Paraska K. K., Ryan C. M. (2006). Cognitive impairment associated with adjuvant therapy in breast cancer. Psychooncology 15, 422–43010.1002/pon.964
    1. Benedict R. H. B. (1997). Brief Visuospatial Memory Test – Revised. Odessa, FL: Psychological Assessment Resources, Inc
    1. Benton A. L., Hamsher K., Sivan A. B. (1994). Multilingual Aphasia Examination, 3rd Edn. Iowa City, IA: AJA
    1. Berglund G., Bolund C., Fornander T., Rutqvist L. E., Sjoden P. (1991). Late effects of adjuvant chemotherapy on quality of life among breast cancer patients. Eur. J. Cancer 27, 1075–108110.1016/0277-5379(91)90295-O
    1. Boone K. B., Miller B. L., Lesser I. M., Hill E., D’Elia L. (1990). Performance on frontal lobe tests in healthy, older individuals. Dev. Neuropsychol. 6, 215–22310.1080/87565649009540462
    1. Brandt J., Benedict R. H. B. (2001). Hopkins Verbal Learning Test – Revised. Professional Manual. Lutz, FL: Psychological Assessment Resources, Inc
    1. Bremner J. D., Southwick S. M., Charney D. S. (1999). “The neurobiology of posttraumatic stress disorder: an integration of animal and human research,” in Posttraumatic Stress Disorder: A Comprehensive Text, eds Saigh P. A., Bremner D. (New York: Allyn and Bacon; ), 103–143
    1. Brezden C., Phillips K. A., Bunston T., Tannock I. F. (2000). Cognitive function in breast cancer patients receiving adjuvant chemotherapy. J. Clin. Oncol. 18, 2695–2701
    1. Brown M. S., Stemmer S. M., Simon J. H., Stears J. C., Jones R. B., Cagnoni P. J., Sheeder J. L. (1998). White matter disease induced by high-dose chemotherapy: longitudinal study with MR imaging and proton spectroscopy. AJNR Am. J. Neuroradiol. 19, 217–221
    1. Buch E. R., Mars R. B., Boorman E. D., Rushworth M. F. (2010). A network centered on ventral premotor cortex exerts both facilitatory and inhibitory control over primary motor cortex during action reprogramming. J. Neurosci. 30, 1395–140110.1523/JNEUROSCI.4882-09.2010
    1. Carlson S., Martinkauppi S., Rama P., Salli E., Korvenoja A., Aronen H. J. (1998). Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. Cereb. Cortex 8, 743–75210.1093/cercor/8.8.743
    1. Castellon S. A., Ganz P. A., Bower J. E., Petersen L., Abraham L., Greendale G. A. (2004). Neurocognitive performance in breast cancer survivors exposed to adjuvant chemotherapy and tamoxifen. J. Clin. Exp. Neuropsychol. 26, 955–96910.1080/13803390490510905
    1. Cimprich B., Reuter-Lorenz P., Nelson J., Clark P. M., Therrien B., Normolle D., Berman M. G., Hayes D. F., Noll D. C., Pelletier S., Welsh R. C. (2010). Prechemotherapy alterations in brain function in women with breast cancer. J. Clin. Exp. Neuropsychol. 32, 324–33110.1080/13803390903032537
    1. Correa D. D., Ahles T. A. (2007). Cognitive adverse effects of chemotherapy in breast cancer patients. Curr. Opin. Support. Palliat. Care 1, 57–6210.1097/SPC.0b013e32813a328f
    1. de Ruiter M. B., Reneman L., Boogerd W., Veltman D. J., van Dam F. S., Nederveen A. J., Boven E., Schagen S. B. (2011). Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Hum. Brain Mapp. 32, 1206–121910.1002/hbm.21102
    1. Denkla M. B. (1993). “Measurement of executive functioning,” in Frames of Reference for the Assessment of Learning Disabilities: New Views on Measurement Issues, ed. Lyon G. R. (Baltimore: Paul Brookes; ), 117–142
    1. Deprez S., Amant F., Yigit R., Porke K., Verhoeven J., Van den Stock J., Smeets A., Christiaens M. R., Leemans A., Van Hecke W., Vandenberghe J., Vandenbulcke M., Sunaert S. (2011). Chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning in breast cancer patients. Hum. Brain Mapp. 32, 480–49310.1002/hbm.21033
    1. Desmond J. E., Chen S. H., DeRosa E., Pryor M. R., Pfefferbaum A., Sullivan E. V. (2003). Increased frontocerebellar activation in alcoholics during verbal working memory: an fMRI study. Neuroimage 19, 1510–152010.1016/S1053-8119(03)00102-2
    1. Dijkstra J. B., Houx P. J., Jolles J. (1999). Cognition after major surgery in the elderly: test performance and complaints. Br. J. Anaesth. 82, 867–874
    1. Dodds C., Allison J. (1998). Postoperative cognitive deficit in the elderly surgical patient. Br. J. Anaesth. 81, 449–462
    1. Durstewitz D., Seamans J. K., Sejnowski T. J. (2000). Neurocomputational models of working memory. Nat. Neurosci. 3(Suppl.), 1184–119110.1038/81460
    1. 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 chemotherapy. J. Clin. Oncol. 25, 3866–387010.1200/JCO.2007.10.8639
    1. Friston K. J., Ashburner J., Poline J. B., Frith C. D., Heather J. D., Frackowiak R. S. J. (1995). Spatial realignment and normalization of images. Hum. Brain Mapp. 2, 165–18910.1002/hbm.460030303
    1. Fuster J. M. (1997). The PFC: Anatomy, Physiology and the Neuropsychology of the Frontal Lobe. New York: Raven Press, 410
    1. Glikmann-Johnston Y., Saling M. M., Chen J., Cooper K. A., Beare R. J., Reutens D. C. (2008). Structural and functional correlates of unilateral mesial temporal lobe spatial memory impairment. Brain 131, 3006–301810.1093/brain/awn213
    1. Goodwin P. J., Ennis M., Pritchard K. I., Trudeau M., Hood N. (1999). Risk of menopause during the first year after breast cancer diagnosis. J. Clin. Oncol. 17, 2365–2370
    1. Gottschalk L. A., Holcombe R. F., Jackson D., Bechtel R. J. (2003). The effects of anticancer chemotherapeutic drugs on cognitive function and other neuropsychiatric dimensions in breast cancer patients. Methods Find. Exp. Clin. Pharmacol. 25, 117–12210.1358/mf.2003.25.2.723685
    1. Gronwall D. M. A. (1997). Paced auditory serial addition task. A measure of recovery from concussion. Percept. Mot. Skills 44, 367–37310.2466/pms.1977.44.2.367
    1. Gualtieri C. T., Johnson L. G. (2006). Reliability and validity of a computerized neurocognitive test battery, CNS vital signs. Arch. Clin. Neuropsychol. 21, 623–64310.1016/j.acn.2006.05.007
    1. Haberecht F., Menon V., Warsofsky I. S., White C. D., Dyer-Friedman J., Glover G. H., Neely E. K., Reiss A. L. (2001). Functional neuroanatomy of visuo-spatial working memory in turner syndrome. Hum. Brain Mapp. 14, 96–10710.1002/hbm.1044
    1. Haley A. P., Gunstad J., Cohen R. A., Jerskey B. A., Mulligan R. C., Sweet L. H. (2008). Neural correlates of visuospatial working memory in healthy young adults at risk for hypertension. Brain Imaging Behav. 2, 192–19910.1007/s11682-008-9025-4
    1. Hurria A., Rosen C., Hudis C., Zuckerman E., Panageas K. S., Lachs M. S., Witmer S., van Gorp W. G., Fornier M., D’Andrea G., Moasser M., Dang C., Van Poznak C., Hurria A., Holland J. (2006). Cognitive function of older patients receiving adjuvant chemotherapy for breast cancer: a pilot prospective longitudinal study. J. Am. Geriatr. Soc. 54, 925–93110.1111/j.1532-5415.2006.00789.x
    1. Inagaki M., Yoshikawa E., Matsuoka Y., Sugawara Y., Nakano T., Akechi T., Wada N., Imoto S., Murakami K., Uchitomi Y. (2007). Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy. Cancer 109, 146–15610.1002/cncr.22368
    1. Jenkins V., Shilling V., Deutsch G., Bloomfield D., Morris R., Allan S., Bishop H., Hodson N., Mitra S., Sadler G., Shah E., Whitehead S., Winstanley J. (2006). A 3-year prospective study of the effects of adjuvant treatments on cognition in women with early stage breast cancer. Br. J. Cancer 94, 828–83410.1038/sj.bjc.6603029
    1. Jonides J., Smith E. E., Koeppe R. A., Awh E., Minoshima S., Mintun M. A. (1993). Spatial working memory in humans as revealed by PET. Nature 363, 623–62510.1038/363623a0
    1. Kesler S. R., Bennett F. C., Mahaffey M. L., Spiegel D. (2009). Regional brain activation during verbal declarative memory in metastatic breast cancer. Clin. Cancer Res. 15, 6665–667310.1158/1078-0432.CCR-09-1227
    1. Kinomura S., Larsson J., Gulyás B., Roland P. E. (1996). Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 26, 512–51510.1126/science.271.5248.512
    1. Kirschbaum C., Hellhammer D. H. (1994). Salivary cortisol in psychoneuroendocrine research – recent developments and applications. Psychoneuroendocrinology 19, 313–33310.1016/0306-4530(94)90013-2
    1. Krampen G. (1991). Fragebogen zu Kompetenz und Kontrollueberzeugungen (FKK). Göttingen: Hogrefe
    1. Krasnow B., Tamm L., Greicius M. D., Yang T. T., Glover G. H., Reiss A. L., Menon V. (2003). Comparison of fMRI activation at 3 and 1.5 T during perceptual, cognitive, and affective processing. Neuroimage 18, 813–82610.1016/S1053-8119(03)00002-8
    1. Kreukels B. P., Hamburger H. L., de Ruiter M. B., van Dam F. S., Ridderinkhof K. R., Boogerd W., Schagen S. B. (2008). ERP amplitude and latency in breast cancer survivors treated with adjuvant chemotherapy. Clin. Neurophysiol. 119, 533–54110.1016/j.clinph.2007.11.011
    1. Kreukels B. P., Schagen S. B., Ridderinkhof K. R., Boogerd W., Hamburger H. L., Muller M. J., van Dam F. S. (2006). Effects of high-dose and conventional-dose adjuvant chemotherapy on long-term cognitive sequelae in patients with breast cancer: an electrophysiologic study. Clin. Breast Cancer 7, 67–7810.3816/CBC.2006.n.015
    1. Kreukels B. P., Schagen S. B., Ridderinkhof K. R., Boogerd W., Hamburger H. L., van Dam F. S. (2005). Electrophysiological correlates of information processing in breast-cancer patients treated with adjuvant chemotherapy. Breast Cancer Res. Treat. 94, 53–6110.1007/s10549-005-7093-3
    1. Lord C., Buss C., Lupien S. J., Pruessner J. C. (2008). Hippocampal volumes are larger in postmenopausal women using estrogen therapy compared to past users, never users and men: a possible window of opportunity effect. Neurobiol. Aging 29, 95–10110.1016/j.neurobiolaging.2006.09.001
    1. Lower E. E., Blau R., Gazder P., Tummala R. (1999). The risk of premature menopause induced by chemotherapy for early breast cancer. J. Womens Health Gend. Based Med. 8, 949–95410.1089/jwh.1.1999.8.949
    1. Lupien S. J., Gillin C. J., Hauger R. L. (1999). Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behav. Neurosci. 113, 420–43010.1037/0735-7044.113.3.420
    1. MacHale S. M., Cavanagh J. T. O., Bennie J., Carroll S., Goodwin G. M., Lawrie S. M. (1998). Diurnal variation of adrenocortical activity in chronic fatigue syndrome. Neuropsychobiology 38, 213–21710.1159/000026543
    1. Maguire E. A., Frith C. D., Burgess N., Donnett J. G., O’Keefe J. (1998). Knowing where things are: parahippocampal involvement in encoding object location in virtual large-scale space. J. Cogn. Neurosci. 10, 61–7610.1162/089892998563789
    1. Maguire E. A., Mummery C. J., Buchel C. (2000). Patterns of hippocampal-cortical interaction dissociate temporal lobe memory subsystems. Hippocampus 10, 475–48210.1002/1098-1063(2000)10:4<475::AID-HIPO14>;2-X
    1. Maier S. F., Watkins L. R. (2003). Immune-to-central nervous system communication and its role in modulating pain and cognition: implications for cancer and cancer treatment. Brain Behav. Immun. 17, 125–13110.1016/S0889-1591(02)00079-X
    1. Mar Fan H. G., Houédé-Tchen N., Yi Q. L., Chemerynsky I., Downie F. P., Sabate K., Tannock I. F. (2005). Fatigue, menopausal symptoms, and cognitive function in women after adjuvant chemotherapy for breast cancer: 1- and 2-year follow-up of a prospective controlled study. J. Clin. Oncol. 31, 8025–8032
    1. 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 Res. Treat. 123, 819–82810.1007/s10549-010-1088-4
    1. McEwen B. (2002). Estrogen actions throughout the brain. Recent Prog. Horm. Res. 57, 357–38410.1210/rp.57.1.357
    1. McEwen B. S. (1999). Stress and the aging hippocampus. Front. Neuroendocrinol. 20, 49–7010.1006/frne.1998.0173
    1. McEwen B. S., Magarinos M. (1997). Stress effects on morphology and function of the hippocampus. Ann. N. Y. Acad. Sci. 821, 271–28410.1111/j.1749-6632.1997.tb48286.x
    1. Monk T. G., Weldon B. C., Garvan C. W., Dede D. E., van der Aa M. T., Heilman K. M., Gravenstein J. S. (2008). Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology 108, 18–3010.1097/01.anes.0000296071.19434.1e
    1. Monteleone P., Maj M. (2009). Circadian rhythm disturbances in depression: implications for reatment and quality of remission. Medicographia 31, 132–139
    1. Noal S., Levy C., Hardouin A., Rieux C., Heutte N., Ségura C., Collet F., Allouache D., Swisters O., Delcambre C., Delozier T., Henry-Amar M., Joly F. (2010). One-year longitudinal study of fatigue, cognitive functions, and quality of life after adjuvant radiotherapy for breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 81, 795–80310.1016/j.ijrobp.2010.06.037
    1. Oei N. Y. L., Everaerd W. T. A. M., Elzinga B. M., van Well S. M., Bermond B. (2006). Psychosocial stress impairs working memory at high loads: an association with cortisol levels and memory retrieval. Stress 9, 133–14110.1080/10253890600965773
    1. Ploner C. J., Gaymard B. M., Rivaud-Pechoux S., Baulac M., Clemenceau S., Severine S., Pierrot-Deseilligny C. (2000). Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb. Cortex 10, 1211–121610.1093/cercor/10.12.1211
    1. Pruessner J. C., Baldwin M. W., Dedovic K., Renwick R., Mahani N. K., Lord C., Meaney M., Lupien S. (2005). Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage 28, 815–82610.1016/j.neuroimage.2005.06.014
    1. Pruessner J. C., Hellhammer D. H., Kirschbaum C. (1999). Low self-esteem, induced failure and the adrenocortical stress response. Pers. Individ. Dif. 27, 477–48910.1016/S0191-8869(98)00256-6
    1. Pruessner J. C., Kirschbaum C., Meinlschmid G., Hellhammer D. H. (2003). Two formulas for the computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28, 916–93110.1016/S0306-4530(02)00108-7
    1. Pruessner J. C., Wolf O. T., Hellhammer D. H., Buske-Kirschbaum A. B., vonAuer K., Jobst S., Kaspers F., Kirschbaum C. (1997). Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 61, 2539–254910.1016/S0024-3205(97)01008-4
    1. 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.” J. Clin. Pharm. Ther. 35, 249–25510.1111/j.1365-2710.2009.01044.x
    1. Rosenberg M. (1985). “Self-concept and psychological well-being in adolescence,” in The Development of the Self, ed. Leahy R. L. (Orlando, FL: The Academic Press; ), 205–246
    1. Sapolsky R. (1985). A possible mechanism for glucocorticoid toxicity in the hippocampus: increased vulnerability of neurons to metabolic insults. J. Neurosci. 5, 1228–1232
    1. Saykin A. J., Ahles T. A., Schoenfeld J. D. (2003). Gray matter reduction on voxel-based morphometry in chemotherapy-treated cancer survivors. J. Int. Neuropsyhol. Soc. 9, 246
    1. Saykin A. J., McDonald B. C., Ahles T., Chesnut L. A., Wang P. J., Furstenberg C. T., Horrigan S. A., Mamourian A. C. (2006). “Altered brain activation following systemic chemotherapy for breast cancer: interim analysis from a prospective fMRI study,” in Abstract presented at 34th Annual Meeting of the International Neuropsychological Society, Boston
    1. Schagen S. B., Muller M. J., Boogerd W., Rosenbrand R. M., van Rhijn D., Rodenhuis S., van Dam F. S. A. M. (2002). Late effects of adjuvant chemotherapy on cognitive function: a follow-up study in breast cancer patients. Ann. Oncol. 132, 1387–139710.1093/annonc/mdf241
    1. Schagen S. B., van Dam F., Muller M. J., Boogerd W., Lindeboom J., Bruning P. F. (1999). Cognitive deficits after postoperative adjuvant chemotherapy for breast carcinoma. Cancer 85, 640–65010.1002/(SICI)1097-0142(19990201)85:3<640::AID-CNCR14>;2-G
    1. Scherwath A., Mehnart A., Schleimer B., Schirmer L., Fehlauer F., Kreienberg R., Metzner B., Thiel E., Zander A. R., Schulz-Kindermann F. (2006). Neuropsychological function in high-risk breast cancer survivors after stem-cell supported high-dose therapy versus standard-dose chemotherapy: evaluation of long-term treatment effects. Ann. Oncol. 17, 415–42310.1093/annonc/mdl051
    1. Schultz W., Apicella P., Ljungberg T. (1993). Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J. Neurosci. 13, 900–913
    1. Servaes P., Verhagen C., Bleijenberg G. (2002). Relations between fatigue, neuropsychological functioning, and physical activity after treatment for breast carcinoma: daily self-report and objective behavior. Cancer 95, 2017–202610.1002/cncr.10891
    1. Shackman A. J., Sarinopoulos I., Maxwell J. S., Pizzagalli D. A., Lavric A., Davidson R. J. (2006). Anxiety selectively disrupts visuospatial working memory. Emotion 6, 40–6110.1037/1528-3542.6.1.40
    1. Shilling V., Jenkins V., Morris R., Deutsch G., Bloomfield D. (2005). The effects of adjuvant chemotherapy on cognition in women with breast cancer – preliminary results of an observational longitudinal study. Breast 14, 142–15010.1016/j.breast.2004.10.004
    1. Shipman S. L., Astur R. S. (2008). Factors affecting the hippocampal BOLD response during spatial memory. Behav. Brain Res. 187, 433–44110.1016/j.bbr.2007.10.014
    1. Shughrue P. J., Merchenthaler I. (2000). Estrogen is more than just a “sex hormone”: novel sites for estrogen action in the hippocampus and cerebral cortex. Front. Neuroendocrinol. 21, 95–10110.1006/frne.1999.0190
    1. Silverman D. H. S., Dy C. J., Castellon S. A., Lai J., Pio B. S., Abraham L., Waddell K., Petersen L., Phelps M. E., Ganz P. A. (2007). Altered frontocortical, cerebellar, and basal ganglia activity in adjuvant-treated breast cancer survivors 5–10 years after chemotherapy. Breast Cancer Res. Treat. 103, 303–31110.1007/s10549-006-9380-z
    1. Smith A. M., Fried P. A., Hogan M. J., Cameron I. (2006). Effects of prenatal marijuana on visuospatial working memory: an fMRI study in young adults. Neurotoxicol. Teratol. 28, 286–29510.1016/j.ntt.2005.12.008
    1. Smith A. M., Longo C. A., Fried P. A., Hogan M. J., Cameron I. (2010). Effects of marijuana on visuospatial working memory: an fMRI study in young adults. Psychopharmacology (Berl.) 210, 429–43810.1007/s00213-010-1841-8
    1. Smith E. E., Jonides J., Koeppe R. A. (1996). Dissociating verbal and spatial working memory using PET. Cereb. Cortex 6, 11–2010.1093/cercor/6.1.11
    1. Spiegel D., Giese-Davis J., Taylor C. B., Kraemer H. (2006). Stress sensitivity in metastatic breast cancer: analysis of hypothalamic-pituitary-adrenal axis function. Psychoneuroendocrinology 31, 1231–124410.1016/j.psyneuen.2006.09.004
    1. Starkman M. N., Gebarski S. S., Berent S., Schteingart D. E. (1992). Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing’s syndrome. Biol. Psychiatry 32, 756–76510.1016/0006-3223(92)90079-F
    1. Stewart A., Collins B., MacKenzie J., Tomiak E., Verma S., Bielajew C. (2007). The cognitive effects of adjuvant chemotherapy in early stage breast cancer: a prospective study. Psychoongology 17, 1–9
    1. Tchen N., Juffs H. G., Downie F. P., Yi Q. L., Hu H., Chemerynsky I., Clemons M., Crump M., Goss P. E., Warr D., Tweedale M. E., Tannock I. F. (2003). Cognitive function, fatigue, and menopausal symptoms in women receiving adjuvant chemotherapy for breast cancer. J. Clin. Oncol. 21, 4175–418310.1200/JCO.2003.01.119
    1. Tuxen M. K., Werner H. S. (1994). Neurotoxicity secondary to antineoplastic drugs. Cancer Treat. Rev. 20, 191–21410.1016/0305-7372(94)90027-2
    1. van Dam F., Schagen S. B., Muller M. J., Boogerd W., Wall E. v. d., Droogleever Fortuyn M. E., Rodenhuis S. (1998). Impairment of cognitive function in women receiving adjuvant treatment for high-risk breast cancer: high-dose versus standard-dose chemotherapy. J. Natl. Cancer Inst. 90, 210–21810.1093/jnci/90.3.210
    1. Vardy J., Booth C., Pond G. R., Zhang H., Galica J., Dhillon H., Clarke S. J., Tannock I. F. (2007). “Cytokine levels in patients with colorectal cancer and breast cancer and their relationship to fatigue and cognitive function,” in Abstract Presented at the American Society of Clinical Oncology- Poster, Patient and Survivor Care, Chicago, IL, 9070
    1. Wagner L. I., Sweet J. J., Butt Z., Desai J., Beaumont J., Havlin K. A., Sabatino T., Cella D. (2006). “Cognitive impairment associated with chemotherapy for breast cancer: an exploratory case-control study,” in Abstract Presented at American Society of Clinical Oncology- Clinical Science Symposium, Cognitive Impairment in Cancer Survivors, Atlanta, GA, 8501
    1. Watanabe M. (1996). Reward expectancy in primate prefrontal neurons. Nature 382, 629–63210.1038/382629a0
    1. Wechsler D. (1997). Wechsler Adult Intelligence Scale, 3rd Edn. San Antonio: Harcourt, Brace, and Co
    1. Wefel J. S., Lenzi R., Theriault R. L., Davis R. N., Meyers C. A. (2004). The cognitive sequelae of standard-dose adjuvant chemotherapy in women with breast carcinoma. Cancer 100, 2292–229910.1002/cncr.20272
    1. Wieneke M. H., Dienst E. R. (1995). Neuropsychological assessment of cognitive functioning following chemotherapy for breast cancer. Psychooncology 4, 61–6610.1002/pon.2960040108

Source: PubMed

3
Tilaa