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Episodic memory in depression: the unique contribution of the anterior caudate and hippocampus

Published online by Cambridge University Press:  06 May 2016

H. K. Jayaweera ,
I. B. Hickie ,
S. L. Duffy ,
L. Mowszowski ,
L. Norrie ,
J. Lagopoulos  and
S. L. Naismith
H. K. Jayaweera
Affiliation:
Healthy Brain Ageing Program, University of Sydney, NSW, Australia Brain and Mind Centre, University of Sydney, NSW, Australia Charles Perkins Centre, University of Sydney, NSW, Australia School of Psychology, University of Sydney, NSW, Australia
I. B. Hickie
Affiliation:
Healthy Brain Ageing Program, University of Sydney, NSW, Australia Brain and Mind Centre, University of Sydney, NSW, Australia
S. L. Duffy
Affiliation:
Healthy Brain Ageing Program, University of Sydney, NSW, Australia Brain and Mind Centre, University of Sydney, NSW, Australia Charles Perkins Centre, University of Sydney, NSW, Australia School of Psychology, University of Sydney, NSW, Australia
L. Mowszowski
Affiliation:
Healthy Brain Ageing Program, University of Sydney, NSW, Australia Brain and Mind Centre, University of Sydney, NSW, Australia Charles Perkins Centre, University of Sydney, NSW, Australia School of Psychology, University of Sydney, NSW, Australia
L. Norrie
Affiliation:
Healthy Brain Ageing Program, University of Sydney, NSW, Australia Brain and Mind Centre, University of Sydney, NSW, Australia
J. Lagopoulos
Affiliation:
Brain and Mind Centre, University of Sydney, NSW, Australia
S. L. Naismith*
Affiliation:
Healthy Brain Ageing Program, University of Sydney, NSW, Australia Brain and Mind Centre, University of Sydney, NSW, Australia Charles Perkins Centre, University of Sydney, NSW, Australia School of Psychology, University of Sydney, NSW, Australia
*
*Address for correspondence: Professor S. L. Naismith, School of Psychology, Brain & Mind Centre & Charles Perkins Centre, University of Sydney, 100 Mallett Street, Camperdown, NSW, Australia. (Email: [email protected])
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Abstract

Background

Learning and memory impairments in older adults with depression are linked to hippocampal atrophy. However, other subcortical regions may also be contributing to these deficits. We aimed to examine whether anterior caudate nucleus volume is significantly reduced in older adults with depression compared to controls; whether anterior caudate volume is associated with performance on tasks of episodic learning and memory, and if so, whether this association is independent of the effects of the hippocampus.

Method

Eighty-four health-seeking participants meeting criteria for lifetime major depressive disorder (mean age = 64.2, s.d. = 9.1 years) and 27 never-depressed control participants (mean age = 63.9, s.d. = 8.0 years) underwent neuropsychological assessment including verbal episodic memory tests [Rey Auditory Verbal Learning Test and Logical Memory (WMS-III)]. Magnetic resonance imaging was conducted, from which subregions of the caudate nucleus were manually demarcated bilaterally and hippocampal volume was calculated using semi-automated methods.

Results

Depressed subjects had smaller right anterior caudate (RAC) (t = 2.3, p = 0.026) and poorer memory compared to controls (t = 2.5, p < 0.001). For depressed subjects only, smaller RAC was associated with poorer verbal memory (r = 0.3, p = 0.003) and older age (r = −0.46, p < 0.001). Multivariable regression showed that the RAC and hippocampus volume uniquely accounted for 5% and 3% of the variance in memory, respectively (β = 0.25, t = 2.16, p = 0.033; β = 0.19, t = 1.71, p = 0.091).

Conclusions

In older people with depression, the anterior caudate nucleus and the hippocampus play independent roles in mediating memory. While future studies examining this structure should include larger sample sizes and adjust for multiple comparisons, these findings support the critical role of the striatum in depression.

Keywords

Caudate nucleusdepressionhippocampusmemory impairment
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 10 , July 2016 , pp. 2189 - 2199
Copyright
Copyright © Cambridge University Press 2016 

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References

APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association Inc.: Washington, DC.Google Scholar
Balleine, BW, O'Doherty, JP (2010). Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35, 48–69.Google Scholar
Ben-Yakov, A, Dudai, Y (2011). Constructing realistic engrams: poststimulus activity of hippocampus and dorsal striatum predicts subsequent episodic memory. Journal of Neuroscience 31, 9032–9042.CrossRefGoogle ScholarPubMed
Butters, MA, Aizenstein, HJ, Hayashi, KM, Meltzer, CC, Seaman, J, Reynolds, CF, Toga, AW, Thompson, PM, Becker, JT, Meltzer, CC, Iii, CFR, Toga, AW, Thompson, PM (2009). Three-dimensional surface mapping of the caudate nucleus in late-life depression. American Journal of Geriatric Psychiatry 17, 4–12.CrossRefGoogle ScholarPubMed
Butters, MA, Young, JB, Lopez, O, Aizenstein, HJ, Mulsant, BH, Reynolds, CF, DeKosky, ST, Becker, JT (2008). Pathways linking late-life depression to persistent cognitive impairment and dementia. Dialogues in Clinical Neuroscience 10, 345–357.CrossRefGoogle ScholarPubMed
Chakos, MH, Lieberman, JA, Bilder, RM, Borenstein, M, Lerner, G, Bogerts, B, Wu, H, Kinon, B, Manzar, A (1994). Increase in caudate nuclei volumes of first-episode schizophrenic patients taking antipsychotic drugs. American Journal of Psychiatry 151, 160.Google Scholar
Diniz, BS, Sibille, E, Ding, Y, Tseng, G, Aizenstein, HJ, Lotrich, F, Becker, JT, Lopez, OL, Lotze, MT, Klunk, WE, Reynolds, CF, Butters, MA (2015). Plasma biosignature and brain pathology related to persistent cognitive impairment in late-life depression. Molecular Psychiatry 20, 594–601.Google Scholar
Duffy, SL, Lagopoulos, J, Hickie, IB, Diamond, K, Graeber, MB, Lewis, SJG, Naismith, SL (2014). Glutathione relates to neuropsychological functioning in mild cognitive impairment. Alzheimer's & Dementia 10, 67–75.Google Scholar
Elcombe, E, Lagopoulos, J, Mowszowski, L, Diamond, K, Paradise, M, Hickie, I, Lewis, S, Naimith, SL (2013). Clinical and cognitive correlates of structural hippocampal change in ‘at risk’ older adults. Journal of Geriatric Psychiatry and Neurology 27, 67–76.Google Scholar
Fedorov, A, Beichel, R, Kalpathy-Cramer, J, Finet, J, Fillion-Robin, JC, Pujol, S, Bauer, C, Jennings, D, Fennessy, F, Sonka, M, Buatti, J, Aylward, S, Miller, JV, Pieper, S, Kikinis, R (2012). 3D Slicer as an image computing platform for the Quantitative Imaging Network, Magnetic Resonance Imaging 30, 1323–1341.Google Scholar
First, MB, Spitzer, RL, Miriam, G, Williams, JB (1996). Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV) . American Psychiatric Press, Inc.: Washington, D.C. Google Scholar
Folstein, MF, Folstein, SE, McHugh, PR (1975). ‘Mini-Mental State’: a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189–198.CrossRefGoogle Scholar
Fossati, P, Coyette, F, Ergis, AM, Allilaire, JF (2002). Influence of age and executive functioning on verbal memory of inpatients with depression. Journal of Affective Disorders 68, 261–271.Google Scholar
Glenthoj, A, Glenthoj, BY, Mackeprang, T, Pagsberg, AK, Hemmingsen, RP, Jernigan, TL, Baaré, WFC (2007). Basal ganglia volumes in drug-naive first-episode schizophrenia patients before and after short-term treatment with either a typical or an atypical antipsychotic drug. Psychiatry Research 154, 199–208.Google Scholar
Griffiths, KR, Morris, RW, Balleine, BW (2014). Translational studies of goal-directed action as a framework for classifying deficits across psychiatric disorders. Frontiers in Systems Neuroscience 8, 1–16.Google Scholar
Hamilton, M (1960). A Rating Scale for Depression. Journal of Neurology, Neurosurgery & Psychiatry 23, 56–62.Google Scholar
Hannestad, J, Taylor, W, McQuoid, DR, Payne, ME, Krishnan, KRR, Steffens, DC, MacFall, JR (2006). White matter lesion volumes and caudate volumes in late-life depression. International Journal of Geriatric Psychiatry 21, 1193–1198.Google Scholar
Hickie, I, Naismith, S, Ward, PB, Turner, K, Scott, E, Mitchell, P, Wilhelm, K, Parker, G (2005). Reduced hippocampal volumes and memory loss in patients with early- and late-onset depression. British Journal of Psychiatry 186, 197–202.Google Scholar
Hickie, I, Scott, E, Naismith, S, Ward, PB, Turner, K, Parker, G, Mitchell, P, Wilhelm, K (2001). Late-onset depression: genetic, vascular and clinical contributions. Psychological Medicine 31, 1403–1412.Google Scholar
Hickie, I, Scott, E, Wilhelm, K, Brodaty, H (1997). Subcortical hyperintensities on magnetic resonance imaging in patients with severe depression – a longitudinal evaluation. Biological Psychiatry 42, 367–374.Google Scholar
Hickie, IB, Naismith, SL, Ward, PB, Scott, EM, Mitchell, PB, Schofield, PR, Scimone, A, Wilhelm, K, Parker, G (2007). Serotonin transporter gene status predicts caudate nucleus but not amygdala or hippocampal volumes in older persons with major depression. Journal of Affective Disorders 98, 137–142.Google Scholar
Jack, CR, Petersen, RC, Xu, Y, O'Brien, PC, Smith, GE, Ivnik, RJ, Tangalos, EG, Kokmen, E (1998). Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease. Neurology 51, 993–999.Google Scholar
Jayaweera, HK, Hickie, IB, Duffy, SL, Hermens, DF, Mowszowski, L, Diamond, K, Terpening, Z, Paradise, M, Lewis, SJG, Lagopoulos, J, Naismith, SL (2015 a). Mild cognitive impairment subtypes in older people with depressive symptoms: relationship with clinical variables and hippocampal change. Journal of Geriatric Psychiatry and Neurology 28, 174–183.Google Scholar
Jayaweera, HK, Lagopoulos, J, Duffy, SL, Lewis, SJG, Hermens, DF, Norrie, L, Hickie, IB, Naismith, SL (2015 b). Spectroscopic markers of memory impairment, symptom severity and age of onset in older people with lifetime depression: discrete roles of N-acetyl aspartate and glutamate. Journal of Affective Disorders 183, 31–38.Google Scholar
Kenny, ER, O'Brien, JT, Cousins, DA, Richardson, J, Thomas, AJ, Firbank, MJ, Blamire, AM (2010). Functional connectivity in late-life depression using resting-state functional magnetic resonance imaging. American Journal of Geriatric Psychiatry 18, 643–651.Google Scholar
Köhler, S, Thomas, AJ, Barnett, NA, O'Brien, JT (2010). The pattern and course of cognitive impairment in late-life depression. Psychological Medicine 40, 591–602.Google Scholar
Lamar, M, Charlton, R, Zhang, A, Kumar, A (2012). Differential associations between types of verbal memory and prefrontal brain structure in healthy aging and late life depression. Neuropsychologia 50, 1823–1829.Google Scholar
Levitt, JJ, McCarley, RW, Dickey, CC, Voglmaier, MM, Niznikiewicz, MA, Seidman, LJ, Hirayasu, Y, Ciszewski, AA, Kikinis, R, Jolesz, FA, Shenton, ME (2002). MRI study of caudate nucleus volume and its cognitive correlates in neuroleptic-naive patients with schizotypal personality disorder. American Journal of Psychiatry 159, 1190–1197.CrossRefGoogle ScholarPubMed
Lezak, M (1982). Neuropsychological Assessment, 2nd edn. Oxford University Press: New York, NY.Google Scholar
Mattfeld, AT, Stark, CEL (2015). Functional contributions and interactions between the human hippocampus and subregions of the striatum during arbitrary associative learning and memory. Hippocampus 25, 900–911.Google Scholar
Miller, MD, Paradis, CF, Houck, PR, Mazumdar, S, Stack, JA, Rifai, H, Mulsant, B, Reynolds, CF III (1992). Rating chronic medical illness burden in geropsychiatric practice and research: application of the Cumulative Illness Rating Scale. Psychiatry Research 41, 237–248.CrossRefGoogle ScholarPubMed
Moon, CM, Yang, JC, Jeong, GW (2015). Explicit verbal memory impairments associated with brain functional deficits and morphological alterations in patients with generalized anxiety disorder. Journal of Affective Disorders 186, 328–336.CrossRefGoogle ScholarPubMed
Naismith, SL, Hickie, I, Ward, PB, Turner, K, Scott, E, Little, C, Mitchell, P, Wilhelm, K, Parker, G (2002). Caudate nucleus volumes and genetic determinants of homocysteine metabolism in the prediction of psychomotor speed in older persons with depression. American Journal of Psychiatry 159, 2096–2098.Google Scholar
Naismith, SL, Hickie, IB, Turner, K, Little, CL, Ward, PB, Wilhelm, K, Mitchell, P, Parker, G, Winter, V (2003). Neuropsychological performance in patients with depression is associated with clinical, etiological and genetic risk factors. Journal of Clinical and Experimental Neuropsychology 25, 866–877.Google Scholar
Naismith, SL, Hickie, IB, Ward, PB, Scott, E, Little, C (2006). Impaired implicit sequence learning in depression: a probe for frontostriatal dysfunction? Psychological Medicine 36, 313–323.Google Scholar
Naismith, SL, Lagopoulos, J, Ward, PB, Davey, CG, Little, C, Hickie, IB (2010). Fronto-striatal correlates of impaired implicit sequence learning in major depression: an fMRI study. Journal of Affective Disorders 125, 256–261.Google Scholar
Naismith, SL, Longley, WA, Scott, EM, Hickie, IB (2007). Disability in major depression related to self-rated and objectively-measured cognitive deficits: a preliminary study. BMC Psychiatry 7, 32.CrossRefGoogle ScholarPubMed
Naismith, SL, Norrie, LM, Mowszowski, L, Hickie, IB (2012). The neurobiology of depression in later-life: clinical, neuropsychological, neuroimaging and pathophysiological features. Progress in Neurobiology 98, 99–143.CrossRefGoogle ScholarPubMed
Naismith, SL, Rogers, NL, Lewis, SJG, Terpening, Z, Ip, T, Diamond, K, Norrie, L, Hickie, IB (2011). Sleep disturbance relates to neuropsychological functioning in late-life depression. Journal of Affective Disorders 132, 139–145.CrossRefGoogle ScholarPubMed
Poldrack, RA, Clark, J, Paré-Blagoev, EJ, Shohamy, D, Creso Moyano, J, Myers, C, Gluck, MA (2001). Interactive memory systems in the human brain. Nature 414, 546–550.Google Scholar
Poldrack, RA, Packard, MG (2003). Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41, 245–251.Google Scholar
Potter, GG, Wagner, HR, Burke, JR, Plassman, BL, Welsh-Bohmer, KA, Steffens, DC (2013). Neuropsychological predictors of dementia in late-life major depressive disorder. American Journal of Geriatric Psychiatry 21, 1–16.Google Scholar
Raz, N, Lindenberger, U, Rodrigue, KM, Kennedy, KM, Head, D, Williamson, A, Dahle, C, Gerstorf, D, Acker, JD (2005). Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cerebral Cortex 15, 1676–1689.Google Scholar
Sexton, CE, McDermott, L, Kalu, UG, Herrmann, LL, Bradley, KM, Allan, CL, Le Masurier, M, Mackay, CE, Ebmeier, KP (2012). Exploring the pattern and neural correlates of neuropsychological impairment in late-life depression. Psychological Medicine 42, 1195–1202.Google Scholar
Shah, PJ, Glabus, MF, Goodwin, GM, Ebmeier, KP (2002). Chronic, treatment-resistant depression and right fronto-striatal atrophy. British Journal of Psychiatry 180, 434–440.Google Scholar
Smith, S, De Stefano, N, Jenkinson, M, Matthews, P (2001). Normalised accurate measurement of longitudinal brain change. Journal of Computer Assisted Tomography 25, 466–475.Google Scholar
Smith, SM, Zhang, Y, Jenkinson, M, Chen, J, Matthews, PM, Federico, A, De Stefano, N (2002). Accurate, robust and automated longitudinal and cross-sectional brain change analysis. NeuroImage 17, 479–489.Google Scholar
Taylor, WD, Aizenstein, HJ, Alexopoulos, GS (2013). The vascular depression hypothesis: mechanisms linking vascular disease with depression. Molecular Psychiatry 18, 963–974.Google Scholar
Voermans, NC, Petersson, KM, Daudey, L, Weber, B, Van Spaendonck, KP, Kremer, HPH, Fernández, G (2004). Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 43, 427–435.CrossRefGoogle ScholarPubMed
Von Gunten, A, Fox, NC, Cipolotti, L, Ron, MA (2000). A volumetric study of hippocampus and amygdala in depressed patients with subjective memory problems. Journal of Neuropsychiatry and Clinical Neurosciences 12, 493–498.Google Scholar
Wechsler, DS (1997). Wechsler Memory Scale, 3rd edn. The Psychological Corporation: San Antonio, TX.Google Scholar
Wechsler, DS (2001). Wechsler Test of Adult Reading. Psychological Corporation: San Antonio, TX.Google Scholar
Yasuno, F, Suhara, T, Nakayama, T, Ichimiya, T, Okubo, Y, Takano, A, Ando, T, Inoue, M, Maeda, J, Suzuki, K (2003). Inhibitory effect of hippocampal 5-HT1A receptors on human explicit memory. American Journal of Psychiatry 160, 334–340.Google Scholar
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