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Fractionation of visuo-spatial memory processes in bipolar depression: a cognitive scaffolding account

Published online by Cambridge University Press:  14 July 2014

P. Gallagher ,
J. M. Gray  and
R. P. C. Kessels
P. Gallagher*
Affiliation:
Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, UK
J. M. Gray
Affiliation:
Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, UK
R. P. C. Kessels
Affiliation:
Donders Institute for Brain Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands Department of Medical Psychology, Radboud University Medical Center, Nijmegen, The Netherlands Vincent van Gogh Institute for Psychiatry, Venray, The Netherlands
*
* Address for correspondence: Dr P. Gallagher, Institute of Neuroscience, Newcastle University, The Henry Wellcome Building, Framlington Place, Newcastle upon Tyne NE2 4HH, UK. (Email: [email protected])
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Abstract

Background

Previous studies of neurocognitive performance in bipolar disorder (BD) have demonstrated impairments in visuo-spatial memory. The aim of the present study was to use an object-location memory (OLM) paradigm to assess specific, dissociable processes in visuo-spatial memory and examine their relationship with broader neurocognitive performance.

Method

Fifty participants (25 patients with BD in a current depressive episode and 25 matched healthy controls) completed the OLM paradigm which assessed three different aspects of visuo-spatial memory: positional memory, object-location binding, and a combined process. Secondary neurocognitive measures of visuo-spatial memory, verbal memory, attention and executive function were also administered.

Results

BD patients were significantly impaired on all three OLM processes, with the largest effect in exact positional memory (d = 1.18, p < 0.0001). General deficits were also found across the secondary neurocognitive measures. Using hierarchical regression, verbal learning was found to explain significant variance on the OLM measures where object-identity was present (the object-location binding and combined processes) and accounted for the group difference. The group difference in precise positional memory remained intact.

Conclusions

This study demonstrates that patients with bipolar depression manifest deficits in visuo-spatial memory, with substantial impairment in fine-grain, positional memory. The differential profile of processes underpinning the visuo-spatial memory impairment suggests a form of ‘cognitive scaffolding’, whereby performance on some measures can be supported by verbal memory. These results have important implications for our understanding of the functional cognitive architecture of mood disorder.

Keywords

Bipolar disorderdepressionneuropsychologyspatial memoryverbal memory
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 3 , February 2015 , pp. 545 - 558
Copyright
Copyright © Cambridge University Press 2014 

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References

Allen, DN, Randall, C, Bello, D, Armstrong, C, Frantom, L, Cross, C, Kinney, J (2010). Are working memory deficits in bipolar disorder markers for psychosis? Neuropsychology 24, 244–254.Google Scholar
Astur, RS, Taylor, LB, Mamelak, AN, Philpott, L, Sutherland, RJ (2002). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research 132, 77–84.Google Scholar
Baddeley, AD, Emslie, H, Nimmo-Smith, I (1992) The Speed and Capacity of Language Processing (SCOLP) Test. Thames Valley Test Company: Bury St Edmunds, Suffolk.Google Scholar
Baddeley, AD, Hitch, G (1974) Working memory. In Recent Advances in Learning and Motivation (ed. Bower, G. A.), pp. 47–90. Academic Press: New York.Google Scholar
Bertolino, A, Frye, M, Callicott, JH, Mattay, VS, Rakow, R, Shelton-Repella, J, Post, R, Weinberger, DR (2003). Neuronal pathology in the hippocampal area of patients with bipolar disorder: a study with proton magnetic resonance spectroscopic imaging. Biological Psychiatry 53, 906–913.Google Scholar
Bird, CM, Burgess, N (2008). The hippocampus and memory: insights from spatial processing. Nature Reviews Neuroscience 9, 182–194.Google Scholar
Bourne, C, Aydemir, O, Balanzá-Martínez, V, Bora, E, Brissos, S, Cavanagh, JTO, Clark, L, Cubukcuoglu, Z, Dias, VV, Dittmann, S, Ferrier, IN, Fleck, DE, Frangou, S, Gallagher, P, Jones, L, Kieseppä, T, Martínez-Aran, A, Melle, I, Moore, PB, Mur, M, Pfennig, A, Raust, A, Senturk, V, Simonsen, C, Smith, DJ, Soares, D, Soeiro-de-Souza, MG, Stoddart, SDR, Sundet, K, Szöke, A, Thompson, JM, Torrent, C, Zalla, T, Craddock, N, Andreassen, OA, Leboyer, M, Vieta, E, Bauer, M, Worhunsky, P, Tzagarakis, C, Rogers, RD, Geddes, JR, Goodwin, GM (2013). Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: an individual patient data meta-analysis. Acta Psychiatrica Scandinavica 128, 149–162.CrossRefGoogle ScholarPubMed
Brown, ES, Rush, AJ, McEwen, BS (1999). Hippocampal remodeling and damage by corticosteroids: implications for mood disorders. Neuropsychopharmacology 21, 474–484.Google Scholar
Cabeza, R, Anderson, ND, Locantore, JK, McIntosh, AR (2002). Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17, 1394–1402.Google Scholar
Cohen, J (1988) Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Dagher, A, Owen, AM, Boecker, H, Brooks, DJ (2001). The role of the striatum and hippocampus in planning: a PET activation study in Parkinson's disease. Brain 124, 1020–1032.Google Scholar
Della Sala, S, Gray, C, Baddeley, A, Allamano, N, Wilson, L (1999). Pattern span: a tool for unwelding visuo-spatial memory. Neuropsychologia 37, 1189–1199.Google Scholar
Dolcos, F, Rice, HJ, Cabeza, R (2002). Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction. Neuroscience & Biobehavioral Reviews 26, 819–825.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Williams, JBW, Gibbon, M (1995) Structured Clinical Interview for DSM-IV (SCID-I), Research Version. Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Forget, H, Lacroix, A, Cohen, H (2002). Persistent cognitive impairment following surgical treatment of Cushing's syndrome. Psychoneuroendocrinology 27, 367–383.CrossRefGoogle ScholarPubMed
Forget, H, Lacroix, A, Somma, M, Cohen, H (2000). Cognitive decline in patients with Cushing's syndrome. Journal of the International Neuropsychological Society 6, 20–29.Google Scholar
Franconeri, SL, Alvarez, GA, Cavanagh, P (2013). Flexible cognitive resources: competitive content maps for attention and memory. Trends in Cognitive Sciences 17, 134–141.Google Scholar
Funahashi, S (2013). Space representation in the prefrontal cortex. Progress in Neurobiology 103, 131–155.Google Scholar
Gallagher, P, Gray, JM, Watson, S, Young, AH, Ferrier, IN (2014). Neurocognitive functioning in bipolar depression: a component structure analysis. Psychological Medicine 44, 961–974.Google Scholar
Gallagher, P, Watson, S, Dye, CE, Young, AH, Ferrier, IN (2008). Persistent effects of mifepristone (RU-486) on cortisol levels in bipolar disorder and schizophrenia. Journal of Psychiatric Research 42, 1037–1041.Google Scholar
Gallagher, P, Watson, S, Smith, MS, Young, AH, Ferrier, (2007). Plasma cortisol-dehydroepiandrosterone (DHEA) ratios in schizophrenia and bipolar disorder. Schizophrenia Research 90, 258–265.Google Scholar
Glahn, DC, Bearden, CE, Cakir, S, Barrett, JA, Najt, P, Monkul, ES, Maples, N, Velligan, DI, Soares, JC (2006). Differential working memory impairment in bipolar disorder and schizophrenia: effects of lifetime history of psychosis. Bipolar Disorders 8, 117–123.Google Scholar
Goswami, U, Sharma, A, Varma, A, Gulrajani, C, Ferrier, IN, Young, AH, Gallagher, P, Thompson, JM, Moore, PB (2009). The neurocognitive performance of drug-free and medicated euthymic bipolar patients do not differ. Acta Psychiatrica Scandinavica 120, 456–463.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology Neurosurgery and Psychiatry 23, 56–62.Google Scholar
Holmes, MK, Erickson, K, Luckenbaugh, DA, Drevets, WC, Bain, EE, Cannon, DM, Snow, J, Sahakian, BJ, Manji, HK, Zarate, CA (2008). A comparison of cognitive functioning in medicated and unmedicated subjects with bipolar depression. Bipolar Disorders 10, 806–815.Google Scholar
Iverson, GL, Brooks, BL, Langenecker, SA, Young, AH (2011). Identifying a cognitive impairment subgroup in adults with mood disorders. Journal of Affective Disorders 132, 360–367.Google Scholar
Judd, LL, Akiskal, HS, Schettler, PJ, Endicott, J, Maser, J, Solomon, DA, Leon, AC, Rice, JA, Keller, MB (2002). The long-term natural history of the weekly symptomatic status of bipolar I disorder. Archives of General Psychiatry 59, 530–537.Google Scholar
Kessels, RP, de Haan, EH, Kappelle, LJ, Postma, A (2001). Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Research Reviews 35, 295–303.Google Scholar
Kessels, RP, de Haan, EH, Kappelle, LJ, Postma, A (2002 a). Selective impairments in spatial memory after ischaemic stroke. Journal of Clinical and Experimental Neuropsychology 24, 115–129.Google Scholar
Kessels, RP, Hendriks, M, Schouten, J, Van Asselen, M, Postma, A (2004). Spatial memory deficits in patients after unilateral selective amygdalohippocampectomy. Journal of the International Neuropsychological Society 10, 907–912.Google Scholar
Kessels, RP, Kappelle, LJ, de Haan, EH, Postma, A (2002 b). Lateralization of spatial-memory processes: evidence on spatial span, maze learning, and memory for object locations. Neuropsychologia 40, 1465–1473.CrossRefGoogle ScholarPubMed
Kessels, RPC, Postma, A (2002). Verbal interference during encoding and maintenance of spatial information in working memory. Current Psychology Letters 3, 9.Google Scholar
Kessels, RPC, Postma, A, de Haan, EHF (1999). Object Relocation: a program for setting up, running, and analyzing experiments on memory for object locations. Behavior Research Methods, Instruments & Computers 31, 423–428.Google Scholar
Kessels, RPC, Postma, A, Kappelle, LJ, de Haan, EHF (2000). Spatial memory impairment in patients after tumour resection: evidence for a double dissociation. Journal of Neurology, Neurosurgery and Psychiatry 69, 389–391.Google Scholar
King, JA, Burgess, N, Hartley, T, Vargha-Khadem, F, O'Keefe, J (2002). Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12, 811–820.Google Scholar
Konradi, C, Zimmerman, EI, Yang, CK, Lohmann, KM, Gresch, P, Pantazopoulos, H, Berretta, S, Heckers, S (2011). Hippocampal interneurons in bipolar disorder. Archives of General Psychiatry 68, 340–350.CrossRefGoogle ScholarPubMed
Kosslyn, SM, Koenig, O, Barrett, A, Cave, CB, Tang, J, Gabrieli, JDE (1989). Evidence for two types of spatial representations: hemispheric specialization for categorical and coordinate relations. Journal of Experimental Psychology: Human Perception and Performance 15, 723–735.Google Scholar
Kurtz, MM, Gerraty, RT (2009). A meta-analytic investigation of neurocognitive deficits in bipolar illness: profile and effects of clinical state. Neuropsychology Review 23, 551–562.CrossRefGoogle ScholarPubMed
Leow, A, Ajilore, O, Zhan, L, Arienzo, D, GadElkarim, J, Zhang, A, Moody, T, Van Horn, J, Feusner, J, Kumar, A, Thompson, P, Altshuler, L (2013). Impaired inter-hemispheric integration in bipolar disorder revealed with brain network analyses. Biological Psychiatry 73, 183–193.CrossRefGoogle ScholarPubMed
Lezak, MD, Howieson, DB, Loring, DW (2004) Neuropsychological Assessment, 4th edn. Oxford University Press: New York.Google Scholar
Macritchie, KA, Lloyd, AJ, Bastin, ME, Vasudev, K, Gallagher, P, Eyre, R, Marshall, I, Wardlaw, JM, Ferrier, IN, Moore, PB, Young, AH (2010). White matter microstructural abnormalities in euthymic bipolar disorder. British Journal of Psychiatry 196, 52–58.Google Scholar
Martinez-Aran, A, Vieta, E, Reinares, M, Colom, F, Torrent, C, Sanchez-Moreno, J, Benabarre, A, Goikolea, JM, Comes, M, Salamero, M (2004). Cognitive function across manic or hypomanic, depressed, and euthymic states in bipolar disorder. American Journal of Psychiatry 161, 262–270.Google Scholar
McGonigle, B, Chalmers, M (2002). A behavior-based fractionation of cognitive competence with clinical applications: a comparative approach. International Journal of Comparative Psychology 15, 154–173.Google Scholar
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382–389.Google Scholar
Park, DC, Reuter-Lorenz, P (2009). The adaptive brain: aging and neurocognitive scaffolding. Annual Review of Psychology 60, 173–196.Google Scholar
Parrot, M, Doyon, B, Demonet, J-F, Cardebat, D (1999). Hemispheric preponderance in categorical and coordinate visual processes. Neuropsychologia 37, 1215–1225.Google Scholar
Postma, A, de Haan, EH (1996). What was where? Memory for object locations. Quarterly Journal of Experimental Psychology A 49, 178–199.Google Scholar
Postma, A, Huntjens, RJC, Meuwissen, M, Laeng, B (2006). The time course of spatial memory processing in the two hemispheres. Neuropsychologia 44, 1914–1918.Google Scholar
Postma, A, Kessels, RPC, van Asselen, M (2004). The neuropsychology of object-location memory. In Remembering Where: Advances in Understanding Spatial Memory (ed. Allen, G.), pp. 143–160. Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Postma, A, Kessels, RPC, van Asselen, M (2008). How the brain remembers and forgets where things are: the neurocognition of object-location memory. Neuroscience and Biobehavioral Reviews 32, 1339–1345.Google Scholar
Rizzo, LB, Costa, LG, Mansur, RB, Swardfager, W, Belangero, SI, Grassi-Oliveira, R, McIntyre, RS, Bauer, ME, Brietzke, E (2014). The theory of bipolar disorder as an illness of accelerated aging: implications for clinical care and research. Neuroscience and Biobehavioral Reviews 42, 157–169.CrossRefGoogle ScholarPubMed
Robbins, TW, James, M, Owen, AM, Sahakian, BJ, Lawrence, AD, McInnes, L, Rabbitt, PM (1998). A study of performance on tests from the CANTAB battery sensitive to frontal lobe dysfunction in a large sample of normal volunteers: implications for theories of executive functioning and cognitive aging. Journal of the International Neuropsychological Society 4, 474–490.CrossRefGoogle Scholar
Robinson, LJ, Ferrier, IN (2006). Evolution of cognitive impairment in bipolar disorder: a systematic review of cross-sectional evidence. Bipolar Disorders 8, 103–116.Google Scholar
Robinson, LJ, Thompson, JM, Gallagher, P, Goswami, U, Young, AH, Ferrier, IN, Moore, PB (2006). A meta-analysis of cognitive deficits in euthymic bipolar subjects. Journal of Affective Disorders 93, 105–115.Google Scholar
Roiser, JP, Cannon, DM, Gandhi, SK, Tavares, JT, Erickson, K, Wood, S, Klaver, JM, Clark, L, Zarate, CA Jr., Sahakian, BJ, Drevets, WC (2009). Hot and cold cognition in unmedicated depressed subjects with bipolar disorder. Bipolar Disorders 11, 178–189.Google Scholar
Rubinsztein, JS, Michael, A, Underwood, BR, Tempest, M, Sahakian, BJ (2006). Impaired cognition and decision-making in bipolar depression but no ‘affective bias’ evident. Psychological Medicine 36, 629–639.Google Scholar
Rybakowski, JK, Twardowska, K (1999). The dexamethasone/corticotropin-releasing hormone test in depression in bipolar and unipolar affective illness. Journal of Psychiatric Research 33, 363–370.Google Scholar
Sarrazin, S, Poupon, C, Linke, J, Wessa, M, Phillips, M, Delavest, M, Versace, A, Almeida, J, Guevara, P, Duclap, D, Duchesnay, E, Mangin, JF, Le Dudal, K, Daban, C, Hamdani, N, D'Albis, MA, Leboyer, M, Houenou, J (2014). A multicenter tractography study of deep white matter tracts in bipolar I disorder: psychotic features and interhemispheric disconnectivity. JAMA Psychiatry 71, 388–396.Google Scholar
Sprooten, E, Sussmann, JE, Clugston, A, Peel, A, McKirdy, J, Moorhead, TWJ, Anderson, S, Shand, AJ, Giles, S, Bastin, ME, Hall, J, Johnstone, EC, Lawrie, SM, McIntosh, AM (2011). White matter integrity in individuals at high genetic risk of bipolar disorder. Biological Psychiatry 70, 350–356.Google Scholar
Steckler, T, Drinkenburg, WH, Sahgal, A, Aggleton, JP (1998). Recognition memory in rats – II. Neuroanatomical substrates. Progress in Neurobiology 54, 313–332.Google Scholar
Sweeney, JA, Kmieca, JA, Kupfer, DJ (2000). Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biological Psychiatry 48, 674–684.CrossRefGoogle ScholarPubMed
Taylor Tavares, JV, Clark, L, Cannon, DM, Erickson, K, Drevets, WC, Sahakian, BJ (2007). Distinct profiles of neurocognitive function in unmedicated unipolar depression and bipolar II depression. Biological Psychiatry 62, 917–924.Google Scholar
van Asselen, M, Kessels, RPC, Kappelle, LJ, Postma, A (2008). Categorical and coordinate spatial representations within object-location memory. Cortex 44, 249–256.Google Scholar
Vanderplas, JM, Garvin, EA (1959). The association value of random shapes. Journal of Experimental Psychology 57, 147–154.Google Scholar
Watson, S, Gallagher, P, Porter, RJ, Smith, MS, Herron, LJ, Bulmer, S, Young, AH, Ferrier, IN (2012). A randomized trial to examine the effect of mifepristone on neuropsychological performance and mood in patients with bipolar depression. Biological Psychiatry 72, 943–949.Google Scholar
Watson, S, Gallagher, P, Ritchie, JC, Ferrier, IN, Young, AH (2004). Hypothalamic-pituitary-adrenal axis function in patients with bipolar disorder. British Journal of Psychiatry 184, 496–502.Google Scholar
Wechsler, D (1981) WAIS-R manual, Wechsler Adult Intelligence Scale-Revised. Psychological Corp: Cleveland, OH.Google Scholar
Werner, S, Diedrichsen, J (2002). The time course of spatial memory distortions. Memory and Cognition 30, 718–730.Google Scholar
Young, AH, Gallagher, P, Watson, S, Del-Estal, D, Owen, BM, Ferrier, IN (2004). Improvements in neurocognitive function and mood following adjunctive treatment with mifepristone (RU-486) in bipolar disorder. Neuropsychopharmacology 29, 1538–1545.Google Scholar
Young, AH, Sahakian, BJ, Robbins, TW, Cowen, PJ (1999). The effects of chronic administration of hydrocortisone on cognitive function in normal male volunteers. Psychopharmacology 145, 260–266.Google Scholar