Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-23T20:28:03.688Z Has data issue: false hasContentIssue false

The association between sleep and cognitive abnormalities in bipolar disorder

Published online by Cambridge University Press:  16 January 2019

A. J. Bradley
Affiliation:
Institute of Neuroscience, Newcastle University, Wolfson Research Centre, Campus for Aging and Vitality, Westgate Road, Newcastle Upon Tyne, NE4 5LP, UK Eli Lilly and Company Limited, Lilly House, Priestly Road, Basingstoke RG24 9NL, UK
K. N. Anderson
Affiliation:
Regional Sleep Service, Freeman Hospital, Freeman Road, High Heaton, Newcastle upon Tyne NE7 7DN, UK
P. Gallagher
Affiliation:
Institute of Neuroscience, Newcastle University, Wolfson Research Centre, Campus for Aging and Vitality, Westgate Road, Newcastle Upon Tyne, NE4 5LP, UK
R. H. McAllister-Williams*
Affiliation:
Institute of Neuroscience, Newcastle University, Wolfson Research Centre, Campus for Aging and Vitality, Westgate Road, Newcastle Upon Tyne, NE4 5LP, UK Northumberland, Tyne and Wear NHS Foundation Trust, Newcastle, UK
*
Author for correspondence: R. H. McAllister-Williams, E-mail: [email protected]

Abstract

Background

Bipolar disorder (BD) is associated with attentional and processing abnormalities. Such abnormalities are also seen in healthy subjects with sleep disruption. We hypothesised cognitive abnormalities in BD patients would be worse in those with objectively verified sleep abnormalities.

Methods

Forty-six BD patients and 42 controls had comprehensive sleep/circadian rhythm assessment over 21 days alongside mood questionnaires. Cognitive function was assessed with a range of tasks including Psychomotor Vigilance Test (PVT), Attention Network Task (ANT) and Digit Symbol Substitution Test (DSST). BD participants with normal and abnormal sleep were compared with age- and sex-matched controls.

Results

BD patients had longer response times and made more lapses (responses >500 ms) than controls on the PVT (both p < 0.001). However, patients with normal sleep patterns did not differ from controls while those with sleep abnormalities did (p < 0.001). An identical pattern of effects were seen with the ANT response times, with the abnormality in bipolar abnormal sleepers related to the executive attentional network. Similarly, patients made fewer correct responses on the DSST compared with the controls (p < 0.001). Bipolar normal sleepers did not differ while those with abnormal sleep did (p < 0.001). All these differences were seen in bipolar abnormal sleepers who were euthymic (p < 0.01) and across the main abnormal sleep phenotypes.

Conclusions

We confirm impairment in attention and processing speed in BD. Rather than sleep abnormalities exacerbating such dysfunction, the impairments were confined to bipolar abnormal sleepers, consistent with sleep disturbance being the main driver of cognitive dysfunction.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

American Academy of Sleep Medicine (2014) International Classification of Sleep Disorders. Darien, Illinois: American Academy of Sleep Medicine.Google Scholar
American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders Fourth Edition (DSM-IV). Washington, DC: American Psychiatric Association.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J and Erbaugh, J (1961) An inventory for measuring depression. Archives of General Psychiatry 4, 561571, Available at http://www.sciencedirect.com/science/article/B6WVB-4F9MR49-1SB/2/ae36a31f5817e3647fa0ff86fab4a2ea.Google Scholar
Bora, E (2018) Neurocognitive features in clinical subgroups of bipolar disorder: a meta-analysis. Journal of Affective Disorders 229, 125134, Available from: PM:29306692.Google Scholar
Bourne, C, Aydemir, O, Balanza-Martinez, V, Bora, E, Brissos, S, Cavanagh, JT, Clark, L, Cubukcuoglu, Z, Dias, VV, Dittmann, S, Ferrier, IN, Fleck, DE, Frangou, S, Gallagher, P, Jones, L, Kieseppa, T, Martinez-Aran, A, Melle, I, Moore, PB, Mur, M, Pfennig, A, Raust, A, Senturk, V, Simonsen, C, Smith, DJ, Bio, DS, Soeiro-de-Souza, MG, Stoddart, SD, Sundet, K, Szoke, A, Thompson, JM, Torrent, C, Zalla, T, Craddock, N, Andreassen, OA, Leboyer, M, Vieta, E, Bauer, M, Worhunsky, PD, Tzagarakis, C, Rogers, RD, Geddes, JR and Goodwin, GM (2013) Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: an individual patient data meta-analysis. Acta Psychiatrica Scandinavica 128, 149162, Available from: PM:23617548.Google Scholar
Bradley, AJ, Webb-Mitchell, R, Hazu, A, Slater, N, Middleton, B, Gallagher, P, McAllister-Williams, H and Anderson, KN (2017) Sleep and circadian rhythm disturbance in bipolar disorder. Psychological Medicine 47, 16781689, Available from: PM:28173893.Google Scholar
Bucks, RS, Olaithe, M and Eastwood, P (2013) Neurocognitive function in obstructive sleep apnoea: a meta-review. Respirology 18, 6170, Available from: PM:22913604.Google Scholar
Buysse, DJ, Reynolds, CF III, Monk, TH, Berman, SR and Kupfer, DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Research 28, 193213, Available from: PM:2748771.Google Scholar
Dinges, DF and Powell, JW (1985) Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behavior Research Methods 17, 652655.Google Scholar
Fan, J, McCandliss, BD, Sommer, T, Raz, A and Posner, MI (2002) Testing the efficiency and independence of attentional networks. Journal of Cognitive Neuroscience 14, 340347.Google Scholar
Gallagher, P, Gray, JM, Watson, S, Young, AH and Ferrier, IN (2014) Neurocognitive functioning in bipolar depression: a component structure analysis. Psychological Medicine 44, 961974, Available from: PM:23800475.Google Scholar
Gallagher, P, Nilsson, J, Finkelmeyer, A, Goshawk, M, Macritchie, KA, Lloyd, AJ, Thompson, JM, Porter, RJ, Young, AH, Ferrier, IN, McAllister-Williams, RH and Watson, S (2015) Neurocognitive intra-individual variability in mood disorders: effects on attentional response time distributions. Psychological Medicine 45, 29852997, Available from: PM:26073667.Google Scholar
Giglio, LM, Magalhaes, PV, Kapczinski, NS, Walz, JC and Kapczinski, F (2010) Functional impact of biological rhythm disturbance in bipolar disorder. Journal of Psychiatric Research 44, 220223, Available from: PM:19758600.Google Scholar
Hamilton, M (1967) Development of a rating scale for primary depressive illness. British Journal of Social & Clinical Psychology 6, 278296.Google Scholar
Harvey, AG, Schmidt, DA, Scarna, A, Semler, CN and Goodwin, GM (2005) Sleep-related functioning in euthymic patients with bipolar disorder, patients with insomnia, and subjects without sleep problems. American Journal of Psychiatry 162, 5057.Google Scholar
Johns, MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14, 540545, Available from: PM:1798888.Google Scholar
Kanady, JC, Soehner, AM, Klein, AB and Harvey, AG (2017) The association between insomnia-related sleep disruptions and cognitive dysfunction during the inter-episode phase of bipolar disorder. Journal of Psychiatric Research 88, 8088, Available from: PM:28088728.Google Scholar
Kaplan, KA, Gruber, J, Eidelman, P, Talbot, LS and Harvey, AG (2011) Hypersomnia in inter-episode bipolar disorder: does it have prognostic significance?. Journal of Affective Disorders 132, 438444, Available from: PM:21489637.Google Scholar
Kaplan, KA, Talbot, LS, Gruber, J and Harvey, AG (2012) Evaluating sleep in bipolar disorder: comparison between actigraphy, polysomnography, and sleep diary. Bipolar Disorder 14, 870879, Available from: PM:23167935.Google Scholar
Keller, MB (2003) Past, present, and future directions for defining optimal treatment outcome in depression: remission and beyond. Journal of the American Medical Association 289, 31523160, Available from: PM:12813121.Google Scholar
Kushida, CA, Littner, MR, Morgenthaler, T, Alessi, CA, Bailey, D, Coleman, J Jr, Friedman, L, Hirshkowitz, M, Kapen, S, Kramer, M, Lee-Chiong, T, Loube, DL, Owens, J, Pancer, JP and Wise, M (2005) Practice parameters for the indications for polysomnography and related procedures: an update for 2005. Sleep, 28, 499521, Available from: PM:16171294.Google Scholar
Lacouture, Y and Cousineau, D (2008) How to use MATLAB to fit the ex-Gaussian and other probability functions to a distribution of response times. Methods for Psychology 4, 3545.Google Scholar
Lezak, MD, Howieson, DB and Loring, DW (2004) Neuropsychological Assessment. Oxford, UK: Oxford University Press.Google Scholar
Lim, J and Dinges, DF (2008) Sleep deprivation and vigilant attention. Annals of the New York Academy of Sciences 1129, 305322, Available from: PM:18591490.Google Scholar
Melo, MC, Garcia, RF, Linhares Neto, VB, Sa, MB, de Mesquita, LM, de Araujo, CF and de Bruin, VM (2016) Sleep and circadian alterations in people at risk for bipolar disorder: a systematic review. Journal of Psychiatric Research 83, 211219, Available from: PM:27661417.Google Scholar
Nelson, HE (1982) The National Adult Reading Test (NART): Test Manual. Windsor, England: NFER Publishing Co.Google Scholar
Pariante, CM, Alhaj, HA, Arulnathan, VE, Gallager, P, Hanson, A, Massey, AE and McAllister-Williams, RH (2012) Central glucocorticoid receptor-medicated effects of the antidepressant citalopram in humans: a study using EEG and cognitive testing. Psychoneuroendocrinology 37, 618628.Google Scholar
Perneger, TV (1998) What's wrong with Bonferroni adjustments. British Medical Journal 316, 12361238, Available from: PM:9553006.Google Scholar
Ratcliff, R (1979) Group reaction time distributions and an analysis of distribution statistics. Psychological Bulletin 86, 446461, Available from: PM:451109.Google Scholar
Robinson, LJ, Thompson, JM, Gallagher, P, Goswami, U, Young, AH, Ferrier, IN and Moore, PB (2006) A meta-analysis of cognitive deficits in euthymic patients with bipolar disorder. Journal of Affective Disorders 93, 105115, Available from: PM:16677713.Google Scholar
Samame, C, Martino, DJ and Strejilevich, SA (2014) Longitudinal course of cognitive deficits in bipolar disorder: a meta-analytic study. Journal of Affective Disorders 164, 130138, Available from: PM:24856566.Google Scholar
Schmiedek, F, Oberauer, K, Wilhelm, O, Suss, HM and Wittmann, WW (2007) Individual differences in components of reaction time distributions and their relations to working memory and intelligence. Journal of Experimental Psychology: General 136, 414429, Available from: PM:17696691.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R and Dunbar, GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59(suppl. 20), 2233, Available from: PM:9881538.Google Scholar
Soreca, I, Buttenfield, JA, Hall, MH and Kupfer, DJ (2015) Screening for obstructive sleep apnea in patients with bipolar I disorder: comparison between subjective and objective measures. Bipolar Disorder 17, 345348, Available from: PM:25187351.Google Scholar
Thompson, JM, Gallagher, P, Hughes, JH, Watson, S, Gray, JM, Ferrier, IN and Young, AH (2005) Neurocognitive impairment in euthymic patients with bipolar affective disorder. British Journal of Psychiatry 186, 3240.Google Scholar
van Hees, VT, Sabia, S, Anderson, KN, Denton, SJ, Oliver, J, Catt, M, Abell, JG, Kivimaki, M, Trenell, MI and Singh-Manoux, A (2015) A novel, open access method to assess sleep duration using a wrist-worn accelerometer. PLoS ONE 10, e0142533, Available from: PM:26569414.Google Scholar
Van Someren, EJ, Swaab, DF, Colenda, CC, Cohen, W, McCall, WV and Rosenquist, PB (1999) Bright light therapy: improved sensitivity to its effects on rest-activity rhythms in Alzheimer patients by application of nonparametric methods. Chronobiology International 16, 505518, Available from: PM:10442243.Google Scholar
Walters, AS, LeBrocq, C, Dhar, A, Hening, W, Rosen, R, Allen, RP and Trenkwalder, C (2003) Validation of the International Restless Legs Syndrome Study Group rating scale for restless legs syndrome. Sleep Medicine 4, 121132, Available from: PM:14592342.Google Scholar
Wechsler, D (1981) WAIS-R Manual, Wechsler Adult Intelligence Scale-Revised. Cleveland, OH: Psychological Corp.Google Scholar
Williams, JB, Kobak, KA, Bech, P, Engelhardt, N, Evans, K, Lipsitz, J, Olin, J, Pearson, J and Kalali, A (2008) The GRID-HAMD: standardization of the Hamilton Depression Rating Scale. International Clinical Psychopharmacology 23, 120129.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE and Meyer, DA (1978) A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435, Available from: PM:728692.Google Scholar