Deficits in hippocampal and anterior cingulate functioning during verbal declarative memory encoding in midlife major depression.

OBJECTIVE Prior studies showed that subjects with major depression have deficits in hippocampal-based verbal declarative memory (e.g., recall of a paragraph) and in hippocampal and prefrontal cortical functioning and structure. The purpose of the present study was to assess hippocampal and prefrontal functioning during performance of a verbal declarative memory task in subjects with midlife major depression. METHOD Subjects with midlife major depression (N=18) and healthy subjects (N=9) underwent positron emission tomography imaging during a control task and verbal encoding of a paragraph. RESULTS During the verbal memory encoding task the comparison subjects, but not the subjects with depression, activated the right hippocampus and prefrontal cortex (anterior cingulate), as well as the cuneus and cerebellum. CONCLUSIONS These results are consistent with a failure of hippocampal and anterior cingulate activation in depression, and they support the hypothesis of deficits in hippocampal and anterior cingulate functioning in depression.

[1]  K. Krishnan,et al.  Hippocampal abnormalities in depression. , 1991, The Journal of neuropsychiatry and clinical neurosciences.

[2]  C. Woolley,et al.  Paradoxical effects of adrenal steroids on the brain: Protection versus degeneration , 1992, Biological Psychiatry.

[3]  M. Raichle,et al.  Subgenual prefrontal cortex abnormalities in mood disorders , 1997, Nature.

[4]  L. Squire,et al.  The primate hippocampal formation: evidence for a time-limited role in memory storage. , 1990, Science.

[5]  H N Wagner,et al.  Paralimbic hypoperfusion in unipolar depression. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[6]  C. Kilts,et al.  Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. , 1984, Science.

[7]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[8]  S. Yi Hippocampal atrophy in major depression: a result of depression-induced neurotoxicity? , 1996 .

[9]  S. Pappatà,et al.  Left prefrontal glucose hypometabolism in the depressed state: a confirmation. , 1990, The American journal of psychiatry.

[10]  Klaus P. Ebmeier,et al.  Cortical grey matter reductions associated with treatment-resistant chronic unipolar depression , 1998, British Journal of Psychiatry.

[11]  D. Rubinow,et al.  Relationship of cortisol hypersecretion to brain CT scan alterations in depressed patients , 1983, Psychiatry Research.

[12]  R. Sapolsky Why Stress Is Bad for Your Brain , 1996, Science.

[13]  C. Mazure,et al.  Development and preliminary psychometric properties of an instrument for the measurement of childhood trauma: The early trauma inventory , 2000, Depression and anxiety.

[14]  Leslie G. Ungerleider,et al.  Age-related reductions in human recognition memory due to impaired encoding. , 1995, Science.

[15]  David C. Steffens,et al.  Structural neuroimaging and mood disorders: Recent findings, implications for classification, and future directions , 1998, Biological Psychiatry.

[16]  J. Danion,et al.  Explicit memory and repetition priming in depression. Preliminary findings. , 1991, Archives of general psychiatry.

[17]  D. Rubinow,et al.  Cortisol hypersecretion and cognitive impairment in depression. , 1984, Archives of general psychiatry.

[18]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  G. Niederehe,et al.  Depression and memory impairment: a meta-analysis of the association, its pattern, and specificity. , 1995, Psychological bulletin.

[20]  J. Mazziotta,et al.  Reduction of prefrontal cortex glucose metabolism common to three types of depression. , 1989, Archives of general psychiatry.

[21]  P. Fox,et al.  Cingulate function in depression: a potential predictor of treatment response , 1997, Neuroreport.

[22]  Karl J. Friston,et al.  The anatomy of melancholia – focal abnormalities of cerebral blood flow in major depression , 1992, Psychological Medicine.

[23]  H. Mayberg,et al.  Frontal lobe dysfunction in secondary depression. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[24]  E. Gould,et al.  Neurogenesis in the Dentate Gyrus of the Adult Tree Shrew Is Regulated by Psychosocial Stress and NMDA Receptor Activation , 1997, The Journal of Neuroscience.

[25]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[26]  M. Meaney,et al.  Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. , 1993, Brain research. Molecular brain research.

[27]  J. Calabrese,et al.  Responses to corticotropin-releasing hormone in the hypercortisolism of depression and Cushing's disease. Pathophysiologic and diagnostic implications. , 1986, The New England journal of medicine.

[28]  C. Nemeroff,et al.  Plasma dexamethasone concentrations and the dexamethasone suppression test , 1990, Biological Psychiatry.

[29]  N. Alpert,et al.  Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  L R Schad,et al.  Quantitative magnetic resonance imaging in geriatric depression and primary degenerative dementia. , 1997, Journal of affective disorders.

[31]  Michael D. Nelson,et al.  Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging : A meta-analytic study , 1998 .

[32]  H. Akil,et al.  Increased evening activation of the hypothalamic-pituitary-adrenal axis in depressed patients. , 1994, Archives of general psychiatry.

[33]  Karl J. Friston,et al.  Activation of the human hippocampal formation during auditory-verbal long-term memory function , 1993, Neuroscience Letters.

[34]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[35]  C. Nemeroff,et al.  Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. , 1996, Endocrinology.

[36]  L. Staib,et al.  Hippocampal volume reduction in major depression. , 2000, The American journal of psychiatry.

[37]  M. Hamilton A RATING SCALE FOR DEPRESSION , 1960, Journal of neurology, neurosurgery, and psychiatry.

[38]  M. Stanton,et al.  Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. , 1988 .

[39]  M. LeMay,et al.  Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. , 1992, The New England journal of medicine.

[40]  R. Dolan,et al.  Depression in Parkinson's disease. A positron emission study. , 1994, The British journal of psychiatry : the journal of mental science.

[41]  André Luxen,et al.  Frontal and parietal metabolic disturbances in unipolar depression , 1994, Biological Psychiatry.

[42]  Lars Nyberg,et al.  Special issue on functional neuroimaging of memory , 2003, Neuropsychologia.

[43]  Herbert Feistel,et al.  Effects of sleep deprivation on the limbic system and the frontal lobes in affective disorders: A study with Tc-99m-HMPAO SPECT , 1991, Psychiatry Research: Neuroimaging.

[44]  John R. Votaw,et al.  Optimization of PET activation studies based on the SNR measured in the 3-D Hoffman brain phantom , 1998, IEEE Transactions on Medical Imaging.

[45]  Bruce S. McEwen,et al.  Repeated stress causes reversible impairments of spatial memory performance , 1994, Brain Research.

[46]  H L Miller,et al.  Positron emission tomography measurement of cerebral metabolic correlates of tryptophan depletion-induced depressive relapse. , 1997, Archives of general psychiatry.

[47]  M. Mintun,et al.  Demonstration in vivo of reduced serotonin responsivity in the brain of untreated depressed patients. , 1996, The American journal of psychiatry.

[48]  T. Cizadlo,et al.  Short-term and long-term verbal memory: a positron emission tomography study. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[49]  L H Staib,et al.  Gender differences in cognitive and neural correlates of remembrance of emotional words. , 2001, Psychopharmacology bulletin.

[50]  W T Carpenter,et al.  Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. , 1992, Archives of general psychiatry.

[51]  H. Akil,et al.  Loss of glucocorticoid fast feedback in depression. , 1991, Archives of general psychiatry.

[52]  Eric Vermetten,et al.  Reduced volume of orbitofrontal cortex in major depression , 2002, Biological Psychiatry.

[53]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Karl J. Friston,et al.  Activation of Human Hippocampal Formation During Memory for Faces: A Pet Study , 1995, Cortex.

[55]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  R. Cabeza,et al.  Functional neuroimaging of memory. , 2003, Neuropsychologia.

[57]  K. Krishnan,et al.  Reduction of orbital frontal cortex volume in geriatric depression , 2000, Biological Psychiatry.

[58]  Y. Sheline 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity , 2000, Biological Psychiatry.

[59]  Eric Vermetten,et al.  Regional brain metabolic correlates of alpha-methylparatyrosine-induced depressive symptoms: implications for the neural circuitry of depression. , 2003, JAMA.

[60]  D. Murphy,et al.  Cognitive processes in depression. , 1981, Archives of general psychiatry.

[61]  Richard S. J. Frackowiak,et al.  Learning to find your way: a role for the human hippocampal formation , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  A R McIntosh,et al.  General and specific brain regions involved in encoding and retrieval of events: what, where, and when. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[64]  Daniel L. Schacter,et al.  The role of hippocampus and frontal cortex in age‐ related memory changes: a PET study , 1996, Neuroreport.

[65]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[66]  H. Blumberg,et al.  Hippocampal and anterior cingulate activation deficits in patients with geriatric depression. , 2001, The American journal of psychiatry.

[67]  M. Smith,et al.  Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. , 1995, Endocrinology.

[68]  Patricia S. Goldman TOPOGRAPHY OF COGNITION: Parallel Distributed Networks in Primate Association Cortex , 1988 .

[69]  J. Bremner,et al.  Structural Changes in the Brain in Depression and Relationship to Symptom Recurrence , 2002, CNS Spectrums.

[70]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[71]  E Mervaala,et al.  Quantitative MRI of the hippocampus and amygdala in severe depression , 2000, Psychological Medicine.

[72]  J. Csernansky,et al.  Hippocampal atrophy in recurrent major depression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[73]  S. Folstein,et al.  Paralimbic frontal lobe hypometabolism in depression associated with Huntington's disease , 1992, Neurology.

[74]  J. Mendels,et al.  Urinary free Cortisol excretion in depression , 1976, Psychological Medicine.

[75]  M. Jarvik,et al.  Memory Functions in Depression: Improvement With Antidepressant Medication , 1976 .

[76]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[77]  James R MacFall,et al.  Hippocampal volume in geriatric depression , 2000, Biological Psychiatry.

[78]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[79]  S. Southwick,et al.  MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. , 2003, The American journal of psychiatry.

[80]  M. Jarvik,et al.  Memory functions in depression. , 1976, Archives of general psychiatry.

[81]  B. McEwen,et al.  Chronic Psychosocial Stress Causes Apical Dendritic Atrophy of Hippocampal CA3 Pyramidal Neurons in Subordinate Tree Shrews , 1996, The Journal of Neuroscience.

[82]  H. Mayberg,et al.  Selective hypometabolism in the inferior frontal lobe in depressed patients with Parkinson's disease , 1990, Annals of neurology.

[83]  M Ashtari,et al.  Hippocampal/amygdala volumes in geriatric depression , 1999, Psychological Medicine.

[84]  R. Post,et al.  Effortful and automatic cognitive processes in depression. , 1986, Archives of general psychiatry.

[85]  Deborah A Yurgelun-Todd,et al.  Hippocampal volume in primary unipolar major depression: a magnetic resonance imaging study , 2000, Biological Psychiatry.

[86]  G M Rose,et al.  Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. , 1996, Behavioral neuroscience.

[87]  B. Mcewen,et al.  Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[88]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[89]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.

[90]  R. Sapolsky,et al.  Hippocampal damage associated with prolonged glucocorticoid exposure in primates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[92]  R. Post,et al.  Prefrontal cortex dysfunction in clinical depression , 1994 .

[93]  Daniel L. Schacter,et al.  Brain regions associated with retrieval of structurally coherent visual information , 1995, Nature.

[94]  C King,et al.  Reproducibility of Resting Cerebral Blood Flow Measurements with H215O Positron Emission Tomography in Humans , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[95]  D. Murphy,et al.  Effort and cognition in depression. , 1982, Archives of general psychiatry.

[96]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[97]  Yvette I. Sheline,et al.  Depression Duration But Not Age Predicts Hippocampal Volume Loss in Medically Healthy Women with Recurrent Major Depression , 1999, The Journal of Neuroscience.

[98]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[99]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[100]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[101]  B. Woods,et al.  Relationships between brain ct scan findings and cortisol in psychotic and nonpsychotic depressed patients , 1989, Biological Psychiatry.

[102]  C. Nemeroff,et al.  Reduced corticotropin releasing factor binding sites in the frontal cortex of suicide victims. , 1988, Archives of general psychiatry.

[103]  H. Roffwarg,et al.  Disrupted 24-hour patterns of cortisol secretion in psychotic depression. , 1973, Archives of general psychiatry.

[104]  David Morganstein,et al.  Cost of lost productive work time among US workers with depression. , 2003, JAMA.

[105]  Olga V. Demler,et al.  The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). , 2003, JAMA.