Mechanisms of Chemotherapy-Induced Cognitive Disorders: Neuropsychological, Pathophysiological, and Neuroimaging Perspectives

Seminars in Clinical Neuropsychiatry

Volumn 8, Issue 4, 2003, Pages 201-216

  Saykin, Andrew J ^a   Ahles, Tim A ^a   McDonald, Brenna C ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; CYCLOPHOSPHAMIDE; CYTOKINE; DEXAMETHASONE; DOXORUBICIN; EPIRUBICIN; ESTROGEN; FLUOROURACIL; GAMMA INTERFERON; GLUCOCORTICOID; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 2; METHOTREXATE; METHYLPREDNISOLONE; PACLITAXEL; STEROID; TAMOXIFEN; VINCRISTINE;

AMNESIA; APATHY; APHASIA; BLOOD BRAIN BARRIER; BRAIN DISEASE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER SURGERY; CARCINOMA; CEREBELLUM DISEASE; CEREBROVASCULAR DISEASE; CHRONIC DISEASE; COGNITIVE DEFECT; CONVULSION; DEMENTIA; DOSE RESPONSE; DROWSINESS; DRUG MECHANISM; DRUG PENETRATION; ELECTROPHYSIOLOGY; FATIGUE; GAIT DISORDER; HEADACHE; HEMIPARESIS; HUMAN; HYPERTENSION; INCONTINENCE; LEARNING DISORDER; LETHARGY; LEUKOENCEPHALOPATHY; LOW DRUG DOSE; MEMORY DISORDER; MENTAL DISEASE; MOOD DISORDER; NECROSIS; NEUROIMAGING; NEUROLOGIC DISEASE; NEUROPATHY; NEUROPSYCHOLOGY; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARESIS; PATHOPHYSIOLOGY; QUALITY OF LIFE; REVIEW; SEIZURE; SENSORY DYSFUNCTION; SLEEP DISORDER; STANDARDIZATION; STROKE; TREATMENT OUTCOME; VISUAL DISORDER; VISUAL IMPAIRMENT;

EID: 0345107251     PISSN: 10843612     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (129)

1. Breast Cancer Facts and Figures 2001-2002. Atlanta: American Cancer Society, 2001
2. Cancer Facts and Figures 2002. Atlanta: American Cancer Society, 2002
3. Henderson IC: Breast cancer. In: Murphy GP, Lawrence WL Jr, Lenhard RE Jr, eds: American Cancer Society Textbook of Clinical Oncology. 2nd ed. Atlanta: American Cancer Society, 1995, pp 198-219
4. Hortobagyi GN: Treatment of breast cancer. N Engl J Med 339:974-984, 1998
5. Early Breast Cancer Trialists' Collaborative Group: Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 351:1451-1467, 1998
6. Keime-Guibert F, Napolitano M, Delattre JY: Neurological complications of radiotherapy and chemotherapy. J Neurol 245:695-708, 1998
7. Ahles TA, Saykin Saykin AJ: Cognitive effects of standard-dose chemotherapy in patients with cancer. Cancer Invest 19:812-820, 2001
8. Meyers CA: Neurocognitive dysfunction in cancer patients. Oncology (Huntingt) 14:75-79 discussion 79, 81-72, 85, 2000
9. Ahles TA, Saykin AJ: Breast cancer chemotherapy-related cognitive dysfunction. Clin Breast Cancer 3:84-90, 2002
10. Olin JJ: Cognitive function after systemic therapy for breast cancer. Oncology 15:613-618, 2001
11. Phillips KA, Bernhard J: Adjuvant breast cancer treatment and cognitive function: current knowledge and research directions. J Natl Cancer Inst 95:190-197, 2003
12. Walch SE, Ahles TA, Saykin AJ: Cognitive sequelae of treatment in children, in Holland JC, Breitbart W, Jacobson PB, et al. (eds), Psycho-Oncology. New York, Oxford University Press, 1998
13. Walch SE, Ahles TA, Saykin AJ: Neuropsychological impact of cancer and cancer treatments, in Holland JC, Breitbart W, Jacobson PB, et al. (eds), Psycho-Oncology. New York, Oxford University Press, 1998
14. Ahles TA, Silberfarb PM, Rundle AC, et al: Quality of life in patients with limited small-cell carcinoma of the lung receiving chemotherapy with or without radiation therapy, for cancer and leukemia group B. Psychother Psychosom 62:193-199, 1994
15. Ahles TA, Tope DM, Furstenberg C, et al: Psychologic and neuropsychologic impact of autologous bone marrow transplant. J Clin Oncol 14:1457-1462, 1996
16. Ahles TA, Silberfarb PM, Herndon J II, et al: Psychologic and neuropsychologic functioning of patients with limited small-cell lung cancer treated with chemotherapy and radiation therapy with or without warfarin: a study by the Cancer and Leukemia Group B. J Clin Oncol 16:1954-1960, 1998
17. Ahles TA, Saykin AJ, Furstenberg CT, et al: Neuropsychologic impact of standard-dose systemic chemotherapy in long-term survivors of breast cancer and lymphoma. J Clin Oncol 20:485-493, 2002
18. Meyers CA, Weitzner M, Byrne K, et al: Evaluation of the neurobehavioral functioning of patients before, during and after bone marrow transplantation. J Clin Oncol 12:802-826, 1994
19. Meyers CA, Byrne KS, Komaki R: Cognitive deficits in patients with small cell lung cancer before and after chemotherapy. Lung Cancer 12:231-235, 1995
20. Saykin AJ, Ahles TA: Commentary on neurocognitive dysfunction in cancer patients. Oncology 14:81-85, 2000
21. Schagen SB, Hamburger HL, Muller MJ, et al: Neurophysiological evaluation of late effects of adjuvant high-dose chemotherapy on cognitive function. Journal of Neurooncol 51:159-165, 2001
22. Schagen SB, van Dam FSAM, Muller MJ, et al: Cognitive deficits after postoperative adjuvant chemotherapy for breast carcinoma. Cancer 85:640-650, 1999
23. Brezden CB, Phillips KA, Abdolell M, et al: Cognitive function in breast cancer patients receiving adjuvant chemotherapy. J Clin Oncol 18:2695-2701, 2000
24. Rodenhuls S, Huitema AD, van Dam FS, et al: High-dose chemotherapy with peripheral blood progenitor cell transplantation in the adjuvant treatment of breast cancer. Cancer J Sc Am 6: S125-S130, 2000
25. Schultz PN, Beck ML, Stava C, et al: Health profiles in 5836 long-term cancer survivors. Int J Cancer 104: 488-495, 2003
26. President's Cancer Panel: Cancer Care Issues in the United States Quality of Care, Quality of Life: Washington, DC: National Cancer Program, National Cancer Institute; 1999
27. Ferrell BR, Hassey Dow K: Quality of life among long-term cancer survivors. Oncology 11:565-576, 1997
28. Eifel P, Axelson JA, Costa J, et al: National Institutes of Health Consensus Development Conference Statement: adjuvant therapy for breast cancer, November 1-3, 2000. J Natl Cancer Inst 93:979-989, 2001
29. Cimprich B: Development of an intervention to restore attention in cancer patients. Cancer Nurs 16:83-92, 1993
30. Sohlberg MM, Mateer CA: Introduction to Cognitive Rehabilitation. New York: Guilford Press, 1989
31. McDougall GJ Jr: Memory improvement program for elderly cancer survivors. Geriatric Nursing 22:185-190, 2001
32. Ferguson RJ, Ahles TA: Brief cognitive-behavioral treatment of chemotherapy-associated attention and memory complaints among breast cancer survivors: pilot outcomes. Cancer Survivorship-Resilience Across the Lifespan: Washington, DC: National Cancer Institute and American Cancer Society; 2002
33. Komaki R, Meyers CA, Shin DM, et al: Evaluation of cognitive function in patients with limited small cell lung cancer prior to and shortly following prophylactic cranial irradiation. Int J Radiat Oncol Biol Phys 33: 179-182, 1995
34. Wieneke MH, Dienst ER: Neuropsychological assessment of cognitive functioning following chemotherapy for breast cancer. Psychooncology 4:61-66, 1995
35. van Dam FSAM, Schagen SB, Muller MJ, et al: Impairment of cognitive function in women receiving adjuvant treatment for high-risk breast cancer: high-dose versus standard-dose chemotherapy. J Natl Cancer Inst 90:210-218, 1998
36. Whedon M, Stearns D, Mills LE: Quality of life of long-term adult survivors of autologous bone marrow transplantation. Oncol Nurs Forum 22:1527-1537, 1995
37. Vigliani MC, Yaya-Tur R, Delattre JY: Combined radiation and chemotherapy-induced disorders of the brain and spinal cord. In: Vinken PJ, Bruyn GW, eds. Handbook of Clinical Neurology. New York, North Holland, 1997, pp 353-370
38. Filley CM: Toxic leukoencephalopathy. Clin Neuropharmacol 22:249-260, 1999
39. Posner JB: Neurologic Complications of Cancer. Philadelphia: Davis, 1995
40. Pavlakis SG, Frank Y, Chusid R: Hypertensive encephalopathy, reversible occipitoparietal encephalopathy, or reversible posterior leukoencephalopathy: three names for an old syndrome. J Child Neurol 14:277-281, 1999
41. Tuxen MK, Werner HS: Neurotoxicity secondary to antineoplastic drugs. Cancer Treat Rev 20:191-214, 1994
42. Troy L, McFarland K, Littman-Power S, et al: Cisplatin-based therapy: a neurological and neuropsychological review. Psychooncology 9:29-39, 2000
43. Madhyastha S, Somayaji SN, Rao MS, et al: Hippocampal brain amines in methotrexate-induced learning and memory deficit. Can J Physiol Pharmacol 80:1076-1084, 2002
44. Barton D, Loprinzi C. Novel approaches to preventing chemotherapy-induced cognitive dysfunction in breast cancer: the art of the possible. Clin Breast Cancer 3, S121-127, 2002
45. Brown MS, Simon JH, Stemmer SM, et al: MR and proton spectroscopy of white matter disease induced by high-dose chemotherapy with bone marrow transplant in advanced breast carcinoma. AJNR Am J Neuroradiol 16:2013-2020, 1995
46. Mosby's Drug Consult. Available at: http://home.md-consult.com/das/drug. Accessed September 22, 2002
47. Delattre JY, Posner JB: Neurological complications of chemotherapy and radiation therapy. In: Aminoff MJ, ed. Neurology and General Medicine. New York: Churchill Livingstone, 1995, 421-445
48. Forsyth PAJ, Cascino TL: Neurological complications of chemotherapy. In: Wiley RG, ed. Neurological Complications of Cancer. New York, Marcel Dekker, 1995, pp 241-266
49. Paganini-Hill A, Clark LJ: Preliminary assessment of cognitive function in breast cancer patients treated with tamoxifen. Breast Cancer Res Treat 64:165-176, 2000
50. Henderson VW: Estrogen, cognition, and a woman's risk of Alzheimer's disease. Am J Med 103:11S-18S, 1997
51. Sherwin BB: Estrogen and cognitive functioning in women. Proc Soc Exp Biol Med 217:17-22, 1998
52. Gibbs RB, Burke AM, Johnson DA: Estrogen replacement attenuates effects of scopolamine and lorazepam on memory acquisition and retention. Horm Behav 34:112-125, 1998
53. Stone DJ, Rozovsky I, Morgan TE, et al: Increased synaptic sprouting in response to estrogen via an apolipoprotein E-dependent mechanism: implications for Alzheimer's disease. J Neurosci 18:3180-3185, 1998
54. McEwen BS, Alves SE: Estrogen actions in the central nervous system. Endocr Rev 20:279-307, 1999
55. McEwen BS, Gould E, Orchinik M, et al: Oestrogens and the structural and functional plasticity of neurons: implications for memory, ageing and neurodegenerative processes. Ciba Found Symp 191:52-66; discussion 66-73, 1995
56. Eberling JL, Wu C, Haan MN, et al. Preliminary evidence that estrogen protects against age-related hippocampal atrophy. Neurolbiol Aging 24:725-732, 2003
57. Shaywitz SE, Shaywitz BA, Pugh KR, et al: Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks. JAMA 281:1197-1202, 1999
58. Rasgon NL, Small GW, Siddarth P, et al: Estrogen use and brain metabolic change in older adults. A preliminary report. Psychiatry Res 107:11-18, 2001
59. Bender CM, Paraska KK, Sereika SM, et al: Cognitive function and reproductive hormones in adjuvant therapy for breast cancer: a critical review. J Pain Symptom Manage 21:407-424, 2001
60. Chen D, Wu CF, Shi B, et al: Tamoxifen and toremifene cause impairment of learning and memory function in mice. Pharmacol Biochem Behav 71:269-276, 2002
61. Koehler PJ: Use of corticosteroids in neuro-oncology. Anticancer Drugs 6:19-33, 1995
62. Martignoni E, Costa A, Sinforlani E, et al: The brain as a target for adrenocortical steroids: cognitive implications. Psychoneuroendocrinology 17:343-354, 1992
63. Lupien SJ, Gillin CJ, Hauger RL: Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behav Neurosci 113:420-430, 1999
64. Maier SF, Watkins LR: Immune-to-central nervous system communication and its role in modulating pain and cognition: implications for cancer and cancer treatment. Brain Behav Immun 17:125-131, 2003
65. Meyers CA: Mood and cognitive disorders in cancer patients receiving cytokine therapy. Adv Exp Med Biol 461:75-81, 1999
66. Baile WF: Neuropsychiatric disorders in cancer patients. Curr Opin Oncol 8:182-187, 1996
67. Meyers CA, Valentine AD: Neurologic and psychiatric adverse effects of immunological therapy. CNS Drugs 3:56-68, 1995
68. Vecht CJ, Keohane C, Menon RS, et al: Acute fatal leukoencephalopathy after interleukin-2 therapy. N Engl J Med 323:1146-1147, 1990
69. Capuron L, Ravaud A, Dantzer R: Timing and specificity of the cognitive changes induced by interleukin-2 and interferon-alpha treatments in cancer patients. Psychosom Med 63:376-386, 2001
70. Reichenberg A, Yirmiya R, Schuld A, et al: Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry 58:445-452, 2001
71. Capuron L, Dantzer R: Cytokines and depression: the need for a new paradigm. Brain Behav Immun 17:119-124, 2003
72. Toga AW, Mazziotta JC: Brain Mapping: The Methods. San Diego: Academic Press; 1996
73. Mazziotta JC, Toga AW, Frackowiak RSJ: Brain Mapping: The Disorders. San Diego: Academic Press; 2000
74. Wishart HA, Saykin AJ, McAllister TW: Functional magnetic resonance imaging: emerging clinical applications. Curr Psychiatry Rep 4:338-345, 2002
75. Korinthenberg R, Palm D: Serial EEG-examinations in children undergoing chemotherapy of ALL according to the Berlin-West-protocol [author's transl]. Klin Padiatr 192:142-149, 1980
76. Mayerhofer K, Bodner K, Saletu B, et al: Paclitaxel does not cause central nervous adverse effects: a prospective vigilance-controlled EEG mapping study in ovarian cancer patients. Wien Klin Wochenschr 112:1007-1013, 2000
77. Ciesielski KT, Lesnik PG, Benzel EC, et al: MRI morphometry of mamillary bodies, caudate nuclei, and prefrontal cortices after chemotherapy for childhood leukemia: multivariate models of early and late developing memory subsystems. Behav Neurosci 113:439-450, 1999
78. Lesnik PG, Ciesielski KT, Hart BL, et al: Evidence for cerebellar-frontal subsystem changes in children treated with intrathecal chemotherapy for leukemia: enhanced data analysis using an effect size model. Arch Neurol 55:1561-1568, 1998
79. Ciesielski KT, Yanofsky R, Ludwig RN, et al: Hypoplasia of the cerebellar vermis and cognitive deficits in survivors of childhood leukemia. Arch Neurol 51:985-993, 1994
80. Cetingul N, Aydinok Y, Kantar M, et al: Neuropsychologic sequelae in the long-term survivors of childhood acute lymphoblastic leukemia. Pediatr Hematol Oncol 16:213-220, 1999
81. Harila-Saari AH, Paakko EL, Vainionpaa LK, et al: A longitudinal magnetic resonance imaging study of the brain in survivors in childhood acute lymphoblastic leukemia. Cancer 83:2608-2617, 1998
82. Kingma A, van Dommelen RI, Mooyaart EL, et al: Slight cognitive impairment and magnetic resonance imaging abnormalities but normal school levels in children treated for acute lymphoblastic leukemia with chemotherapy only. J Pediatr 139:413-420, 2001
83. Mulhern RK, Reddick WE, Palmer SL, et al: Neurocognitive deficits in medulloblastoma survivors and white matter loss. Ann Neurol 46:834-841, 1999
84. Mulhern RK, Palmer SL, Reddick WE, et al: Risks of young age for selected neurocognitive deficits in medulloblastoma are associated with white matter loss. J Clin Oncol 19:472-479, 2001
85. Hook CC, Kimmel DW, Kvols LK, et al: Multifocal inflammatory leukoencephalopathy with 5-fluorouracil and levamisole. Ann Neurol 31:262-267, 1992
86. Kimmel DW, Wijdicks EF, Rodriguez M: Multifocal inflammatory leukoencephalopathy associated with levamisole therapy. Neurology 45:374-376, 1995
87. Brown US, Stemmer SM, Simon JH, et al: White matter disease induced by high-dose chemotherapy: longitudinal study with MR imaging and proton spectroscopy. AJNR Am J Neuroradiol 19:217-221, 1998
88. Basser PJ, Mattiello J, Le Bihan D: MR diffusion tensor spectroscopy and imaging. Biophys J 66:259-267, 1994
89. Nakada T: Functionality and connectivity analysis by magnetic resonance imaging. Rinsho Shinkeigaku 37: 1155-1157, 1997
90. Pierpaoli C, Jezzard P, Basser PJ, et al: Diffusion tensor MR imaging of the human brain. Radiology 201:637-648, 1996
91. Le Bihan D, Mangin JF, Poupon C, et al: Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534-546, 2001
92. Werring DJ, Clark CA, Barker GJ, et al: The structural and functional mechanisms of motor recovery: complementary use of diffusion tensor and functional magnetic resonance imaging in traumatic injury of the internal capsule. J Neurol Neurosurg Psychiatry 65: 863-869, 1998
93. Werring DJ, Clark CA, Parker GJ, et al: A direct demonstration of both structure and function in the visual system: combining diffusion tensor imaging with functional magnetic resonance imaging. Neuroimage 9:352-361, 1999
94. O'Sullivan M, Summers PE, Jones DK, et al: Normal-appearing white matter in ischemic leukoariosis: a diffusion tensor MRI study. Neurology 57:2307-2310, 2001
95. Jones DK, Lythgoe D, Horsfield MA, et al: Characterization of white matter damage in ischemic leukoariosis with diffusion tensor MRI. Stroke 30:393-397, 1999
96. Iannucci G, Rovaris M, Giacomotti L, et al: Correlation of multiple sclerosis measures derived from T2-weighted, T1-weighted, magnetization transfer, and diffusion tensor MR imaging. AJNR Am J Neuroradiol 22:1462-1467, 2001
97. Bozzali M, Franceschi M, Falini A, et al: Quantification of tissue damage in AD using diffusion tensor and magnetization transfer MRI. Neurology 57:1135-1137, 2001
98. Lim KO, Hedehus M, Moseley M, et al: Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry 56:367-374, 1999
99. Buchsbaum MS, Tang CY, Peled S, et al: MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia. Neuroreport 9:425-43, 1998
100. Arfanakis K, Hermann BP, Rogers BP, et al: Diffusion tensor MRI in temporal lobe epilepsy. Magn Reson Imaging 20:511-519, 2002
101. Arfanakis K, Haughton VM, Carew JD, et al: Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am J Neuroradiol 23:794-802, 2002
102. Sabri O, Ringelstein EB, Hellwig D, et al: Neuropsychological impairment correlates with hypoperfusion and hypometabolism but not with severity of white matter lesions on MRI in patients with cerebral microangiopathy. Stroke 30:556-566, 1999
103. Fulham MJ, Brunetti A, Aloj L, et al: Decreased cerebral glucose metabolism in patients with brain tumors: an effect of corticosteroids. J Neurosurg 83:657-664, 1995
104. Khiat A, Bard C, Lacroix A, et al: Brain metabolic alterations in Cushing's syndrome as monitored by proton magnetic resonance spectroscopy. NMR Biomed 12:357-363, 1999
105. Khiat A, Yared Z, Bard C, et al: Long-term brain metabolic alterations in exogenous Cushing's syndrome as monitored by proton magnetic resonance spectroscopy. Brain Res 911:134-140, 2001
106. Bandettini PA, Wong EC: Magnetic resonance imaging of human brain function. Principles, practicalities, and possibilities. Neurosurg Clin N Am 8:345-371, 1997
107. Rosen BR, Buckner RL, Dale AM: Event-related functional MRI: past, present, and future. Proc Natl Acad Sci U S A 95:773-780, 1998
108. Moonen CTW, Bandettini PA, eds. Functional MRI. Berlin, New York: Springer, 2000
109. Saykin AJ, Riordan HJ, Burr RB, et al: Functional magnetic resonance imaging: studies of memory, in Bigler ED (ed.) Neuroimaging II: Clinical Applications. New York, Plenum Press, 1996, pp 331-348
110. Belliveau JW, Kwong KK, Kennedy DN, et al: Magnetic resonance imaging mapping of brain function. Human visual cortex. Invest Radiol 27:S59-S65, 1992
111. Kwong KK, Belliveau JW, Chesler DA, et al: Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci U S A 89:5675-5679, 1992
112. Ogawa S, Menon RS, Kim SG, et al: On the characteristics of functional magnetic resonance imaging of the brain. Annual Review of Biophysics & Biomolecular Structure 27:447-474, 1998
113. Logothetis NK, Pauls J, Augath M, et al: Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157, 2001
114. Lai S, Hopkins AL, Haake EM, et al: Identification of vascular structures as a major source of signal contrast in high resolution 2D and 3D functional activation imaging of the motor cortex at 1.5T: preliminary results. Magn Reson Med 30:387-392, 1993
115. Bandettini PA, Jesmanowicz A, Wong EC, et al: Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30:161-173, 1993
116. D'Esposito M, Zarahn E, Aguirre GK, et al: The effect of normal aging on the coupling of neural activity to the bold hemodynamic response. Neuroimage 10:6-14, 1999
117. Johnson SC, Saykin AJ, Flashman LA, et al: Similarities and differences in semantic and phonological processing with age: patterns of functional MRI activation. Aging, Neuropsychology, and Cognition 8:307-320, 2001
118. Ross MH, Yurgelun-Todd DA, Renshaw PF, et al: Age-related reduction in functional MRI response to photic stimulation. Neurology 48:173-176, 1997
119. Ashburner J, Friston KF: Voxel-based morphometry-the methods. Neuroimage 11:805-821, 2000
120. Good CD, Johnsrude IS, Ashburner J, et al: A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21-36, 2001
121. Baron JC, Chetelat G, Desgranges B, et al: In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. Neuroimage 14:298-309, 2001
122. Chetelat G, Desgranges B, de la Sayette V, et al: Mapping gray matter loss with voxel-based morphometry in mild cognitive impairment. Neuroreport 13:1939-1943, 2002
123. Saykin AJ, Wishart HA: Mild cognitive impairment: conceptual issues and structural and functional brain correlates. Semin Clin Neuropsychiatry 8:12-30, 2003
124. Saykin AJ, Wishart HA, Santulli R, et al: Relation of decreased gray matter volume to verbal learning and subjective memory complaints in healthy older adults and patients with mild cognitive impairment. J Neuropsychiatry Clin Neurosci 15:263, 2003
125. Kubicki M, Shenton ME, Salisbury DF, et al: Voxel-based morphometric analysis of gray matter in first episode schizophrenia. Neuroimage 17:1711-1719, 2002
126. Woermann FG, Free SL, Koepp MJ, et al: Voxel-by-voxel comparison of automatically segmented cerebral gray matter-a rater-independent comparison of structural MRI in patients with epilepsy. Neuroimage 10:373-384, 1999
127. McDonald BC, Wishart HA, Saykin AJ, et al: Gray matter reduction on voxel-based morphometry in multiple sclerosis. J Int Neuropsychol Soc 9:228, 2003
128. Greenlee BA, Wishart HA, McDonald BC, et al: Right frontal white and gray matter volumes correlate with depressive symptoms in MS. J Neuropsychiatry Clin Neurosci 2003
129. Saykin AJ, Ahles TA, Schoenfeld JD, et al: Gray matter reduction on voxel-based morphometry in chemotherapy-treated cancer survivors. J Int Neuropsychol Soc 9: 246, 2003