Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-24T16:11:24.753Z Has data issue: false hasContentIssue false

Effect of high-endurance exercise intervention on sleep-dependent procedural memory consolidation in individuals with schizophrenia: a randomized controlled trial

Published online by Cambridge University Press:  07 October 2021

Lincoln Lik Hang Lo
Affiliation:
Department of Psychiatry, University of Hong Kong, Pok Fu Lam, Hong Kong
Edwin Ho Ming Lee*
Affiliation:
Department of Psychiatry, University of Hong Kong, Pok Fu Lam, Hong Kong
Christy Lai Ming Hui
Affiliation:
Department of Psychiatry, University of Hong Kong, Pok Fu Lam, Hong Kong
Catherine Shiu Yin Chong
Affiliation:
Department of Psychiatry, Kwai Chung Hospital, Kwai Chung, Hong Kong
Wing Chung Chang
Affiliation:
Department of Psychiatry, University of Hong Kong, Pok Fu Lam, Hong Kong State Key Laboratory of Brain and Cognitive Sciences, University of Hong Kong, Pok Fu Lam, Hong Kong
Sherry Kit Wa Chan
Affiliation:
Department of Psychiatry, University of Hong Kong, Pok Fu Lam, Hong Kong State Key Laboratory of Brain and Cognitive Sciences, University of Hong Kong, Pok Fu Lam, Hong Kong
Jessie Jingxia Lin
Affiliation:
Neuroscience and Neurological Rehabilitation, The Hong Kong Polytechnic University, Hung Hom, Hong Kong
William Tak Lam Lo
Affiliation:
Department of Psychiatry, Kwai Chung Hospital, Kwai Chung, Hong Kong
Eric Yu Hai Chen
Affiliation:
Department of Psychiatry, University of Hong Kong, Pok Fu Lam, Hong Kong State Key Laboratory of Brain and Cognitive Sciences, University of Hong Kong, Pok Fu Lam, Hong Kong
*
Author for correspondence: Edwin Ho Ming Lee, E-mail: edwinlhm@hku.hk

Abstract

Background

Little is known about the effects of physical exercise on sleep-dependent consolidation of procedural memory in individuals with schizophrenia. We conducted a randomized controlled trial (RCT) to assess the effectiveness of physical exercise in improving this cognitive function in schizophrenia.

Methods

A three-arm parallel open-labeled RCT took place in a university hospital. Participants were randomized and allocated into either the high-intensity-interval-training group (HIIT), aerobic-endurance exercise group (AE), or psychoeducation group for 12 weeks, with three sessions per week. Seventy-nine individuals with schizophrenia spectrum disorder were contacted and screened for their eligibility. A total of 51 were successfully recruited in the study. The primary outcome was sleep-dependent procedural memory consolidation performance as measured by the finger-tapping motor sequence task (MST). Assessments were conducted during baseline and follow-up on week 12.

Results

The MST performance scored significantly higher in the HIIT (n = 17) compared to the psychoeducation group (n = 18) after the week 12 intervention (p < 0.001). The performance differences between the AE (n = 16) and the psychoeducation (p = 0.057), and between the AE and the HIIT (p = 0.999) were not significant. Yet, both HIIT (p < 0.0001) and AE (p < 0.05) showed significant within-group post-intervention improvement.

Conclusions

Our results show that HIIT and AE were effective at reverting the defective sleep-dependent procedural memory consolidation in individuals with schizophrenia. Moreover, HIIT had a more distinctive effect compared to the control group. These findings suggest that HIIT may be a more effective treatment to improve sleep-dependent memory functions in individuals with schizophrenia than AE alone.

Type
Original Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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

Adriano, F., Caltagirone, C., & Spalletta, G. (2012). Hippocampal volume reduction in first-episode and chronic schizophrenia: A review and meta-analysis. Neuroscientist, 18(2), 180200. doi: 10.1177/1073858410395147CrossRefGoogle ScholarPubMed
Albouy, G., King, B. R., Maquet, P., & Doyon, J. (2013). Hippocampus and striatum: Dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus, 23(11), 9851004. doi: 10.1002/hipo.22183CrossRefGoogle ScholarPubMed
Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T., … Maquet, P. (2008). Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron, 58(2), 261272. doi: 10.1016/j.neuron.2008.02.008CrossRefGoogle ScholarPubMed
Allen, H., & Coggan, A. R. (2010). Training and racing with a power meter (2nd ed.). Boulder, CO: VeloPress.Google Scholar
Andreasen, N. C. (1991). Dementia Praecox and Paraphrenia – Kraepelin, E. American Journal of Psychiatry, 148(12), 17311733.Google Scholar
Baron, K. G., Reid, K. J., & Zee, P. C. (2013). Exercise to improve sleep in insomnia: Exploration of the bidirectional effects. Journal of Clinical Sleep Medicine, 9(8), 819824. doi: 10.5664/jcsm.2930CrossRefGoogle ScholarPubMed
Boecker, H., Dagher, A., Ceballos-Baumann, A. O., Passingham, R. E., Samuel, M., Friston, K. J., … Brooks, D. J. (1998). Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: Investigations with H2 15O PET. Journal of Neurophysiology, 79(2), 10701080. doi: 10.1152/jn.1998.79.2.1070CrossRefGoogle ScholarPubMed
Booth, M. (2000). Assessment of physical activity: An international perspective (vol. 71, pp. 114, 2000). Research Quarterly for Exercise and Sport, 71(3), 312312.CrossRefGoogle Scholar
Boyer, P., Phillips, J. L., Rousseau, F. L., & Ilivitsky, S. (2007). Hippocampal abnormalities and memory deficits: New evidence of a strong pathophysiological link in schizophrenia. Brain Research Reviews, 54(1), 92112. doi: 10.1016/j.brainresrev.2006.12.008CrossRefGoogle Scholar
Cahill, L. (2006). Why sex matters for neuroscience. Nature Reviews Neuroscience, 7(6), 477484. doi: 10.1038/nrn1909CrossRefGoogle ScholarPubMed
Chung, K. F., Kan, K. K., & Yeung, W. F. (2011). Assessing insomnia in adolescents: Comparison of insomnia severity index, Athens insomnia scale and sleep quality index. Sleep Medicine, 12(5), 463470. doi: 10.1016/j.sleep.2010.09.019CrossRefGoogle ScholarPubMed
Chung, K. F., & Tang, M. K. (2006). Subjective sleep disturbance and its correlates in middle-aged Hong Kong Chinese women. Maturitas, 53(4), 396404. doi: 10.1016/j.maturitas.2005.07.001CrossRefGoogle ScholarPubMed
Coggan, A. R., Kohrt, W. M., Spina, R. J., Kirwan, J. P., Bier, D. M., & Holloszy, J. O. (1992). Plasma glucose kinetics during exercise in subjects with high and low lactate thresholds. Journal of Applied Physiology (1985), 73(5), 18731880.CrossRefGoogle ScholarPubMed
de Aquino-Lemos, V., Santos, R. V., Antunes, H. K., Lira, F. S., Luz Bittar, I. G., Caris, A. V., … de Mello, M. T. (2016). Acute physical exercise under hypoxia improves sleep, mood and reaction time. Physiology & Behavior, 154, 9099. doi: 10.1016/j.physbeh.2015.10.028CrossRefGoogle ScholarPubMed
Denham, J., Scott-Hamilton, J., Hagstrom, A. D., & Gray, A. J. (2020). Cycling power outputs predict functional threshold power and maximum oxygen uptake. The Journal of Strength and Conditioning Research, 34(12), 34893497. doi: 10.1519/JSC.0000000000002253CrossRefGoogle ScholarPubMed
Doyon, J., & Benali, H. (2005). Reorganization and plasticity in the adult brain during learning of motor skills. Current Opinion in Neurobiology, 15(2), 161167. doi: 10.1016/j.conb.2005.03.004CrossRefGoogle ScholarPubMed
Eich, T. S., & Metcalfe, J. (2009). Effects of the stress of marathon running on implicit and explicit memory. Psychonomic Bulletin & Review, 16(3), 475479. doi: 10.3758/PBR.16.3.475CrossRefGoogle ScholarPubMed
Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1(1), 4150. doi: 10.1038/35036213CrossRefGoogle ScholarPubMed
Fukuzako, H., Fukazako, T., Hashiguchi, T., Hokazono, Y., Takeuchi, K., Hirakawa, K., … Fujimoto, T. (1996). Reduction in hippocampal formation volume is caused mainly by its shortening in chronic schizophrenia: Assessment by MRI. Biological Psychiatry, 39(11), 938945.CrossRefGoogle ScholarPubMed
Genzel, L., Kiefer, T., Renner, L., Wehrle, R., Kluge, M., Grozinger, M., … Dresler, M. (2012). Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology, 37(7), 987998. doi: 10.1016/j.psyneuen.2011.11.006CrossRefGoogle ScholarPubMed
Genzel, L., Rossato, J. I., Jacobse, J., Grieves, R. M., Spooner, P. A., Battaglia, F. P., … Morris, R. G. (2017). The Yin and Yang of memory consolidation: Hippocampal and neocortical. PLoS Biology, 15(1), e2000531. doi: 10.1371/journal.pbio.2000531CrossRefGoogle ScholarPubMed
He, Y., Cornelissen-Guillaume, G. G., He, J., Kastin, A. J., Harrison, L. M., & Pan, W. (2016). Circadian rhythm of autophagy proteins in hippocampus is blunted by sleep fragmentation. Chronobiology International, 33(5), 553560. doi: 10.3109/07420528.2015.1137581CrossRefGoogle ScholarPubMed
Heckers, S., Rauch, S. L., Goff, D., Savage, C. R., Schacter, D. L., Fischman, A. J., & Alpert, N. M. (1998). Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience, 1(4), 318323. doi: 10.1038/1137CrossRefGoogle ScholarPubMed
Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002). Central mechanisms of motor skill learning. Current Opinion in Neurobiology, 12(2), 217222.CrossRefGoogle ScholarPubMed
Jenkins, I. H., Brooks, D. J., Nixon, P. D., Frackowiak, R. S., & Passingham, R. E. (1994). Motor sequence learning: A study with positron emission tomography. The Journal of Neuroscience, 14(6), 37753790.CrossRefGoogle ScholarPubMed
Joo, E. Y., Kim, H., Suh, S., & Hong, S. B. (2014). Hippocampal substructural vulnerability to sleep disturbance and cognitive impairment in patients with chronic primary insomnia: Magnetic resonance imaging morphometry. Sleep, 37(7), 11891198. doi: 10.5665/sleep.3836CrossRefGoogle ScholarPubMed
Karni, A., Meyer, G., Rey-Hipolito, C., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1998). The acquisition of skilled motor performance: Fast and slow experience-driven changes in primary motor cortex. Proceedings of the National Academy of Sciences of the United States of America, 95(3), 861868.CrossRefGoogle ScholarPubMed
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261276, doi:10.1093/schbul/13.2.261.CrossRefGoogle ScholarPubMed
Kimhy, D., Lauriola, V., Bartels, M. N., Armstrong, H. F., Vakhrusheva, J., Ballon, J. S., & Sloan, R. P. (2016). Aerobic exercise for cognitive deficits in schizophrenia — The impact of frequency, duration, and fidelity with target training intensity. Schizophrenia Research, 172(1-3), 213215. http://dx.doi.org/10.1016/j.schres.2016.01.055CrossRefGoogle ScholarPubMed
Lalande, D., Theriault, L., Kalinova, E., Fortin, A., & Leone, M. (2016). The effect of exercise on sleep quality and psychological, physiological, and biological correlates in patients with schizophrenia: A pilot study. Schizophrenia Research, 171(1–3), 235236. doi: 10.1016/j.schres.2016.01.042CrossRefGoogle ScholarPubMed
Lieberman, J. A., Stroup, T. S., McEvoy, J. P., Swartz, M. S., Rosenheck, R. A., Perkins, & D. O., … Clinical Antipsychotic Trials of Intervention Effectiveness, I. (2005). Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. The New England Journal of Medicine, 353(12), 12091223. doi:10.1056/NEJMoa051688CrossRefGoogle ScholarPubMed
Lin, J., Chan, S. K., Lee, E. H., Chang, W. C., Tse, M., Su, W. W., … Chen, E. Y. (2015). Aerobic exercise and yoga improve neurocognitive function in women with early psychosis. NPJ Schizophrenia, 1(0), 15047. doi: 10.1038/npjschz.2015.47CrossRefGoogle ScholarPubMed
Loprinzi, P. D., & Frith, E. (2018). The role of sex in memory function: Considerations and recommendations in the context of exercise. Journal of Clinical Medicine, 7(6), 132. doi: 10.3390/jcm7060132CrossRefGoogle ScholarPubMed
Maculano Esteves, A., Ackel-D'Elia, C., Tufik, S., & De Mello, M. T. (2014). Sleep patterns and acute physical exercise: The effects of gender, sleep disturbances, type and time of physical exercise. The Journal of Sports Medicine and Physical Fitness, 54(6), 809815.Google ScholarPubMed
Manoach, D. S., Cain, M. S., Vangel, M. G., Khurana, A., Goff, D. C., & Stickgold, R. (2004). A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia. Biological Psychiatry, 56(12), 951956. doi: 10.1016/j.biopsych.2004.09.012CrossRefGoogle ScholarPubMed
Manoach, D. S., & Stickgold, R. (2009). Does abnormal sleep impair memory consolidation in schizophrenia? Frontiers in Human Neuroscience, 3, 21. doi: 10.3389/neuro.09.021.2009CrossRefGoogle ScholarPubMed
Manoach, D. S., Thakkar, K. N., Stroynowski, E., Ely, A., McKinley, S. K., Wamsley, E., … Stickgold, R. (2010). Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. Journal of Psychiatric Research, 44(2), 112120. doi: 10.1016/j.jpsychires.2009.06.011CrossRefGoogle ScholarPubMed
Martin, J. C., Milliken, D. L., Cobb, J. E., McFadden, K. L., & Coggan, A. R. (1998). Validation of a mathematical model for road cycling power. Journal of Applied Biomechanics, 14(3), 276291. doi: 10.1123/jab.14.3.276CrossRefGoogle ScholarPubMed
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review, 102(3), 419457.CrossRefGoogle ScholarPubMed
McNaughton, N., & Wickens, J. (2003). Hebb, pandemonium and catastrophic hypermnesia: The hippocampus as a suppressor of inappropriate associations. Cortex, 39(4–5), 11391163.CrossRefGoogle ScholarPubMed
Monnet, F. P. (2002). Melatonin modulates [3H]serotonin release in the rat hippocampus: Effects of circadian rhythm. Journal of Neuroendocrinology, 14(3), 194199.CrossRefGoogle ScholarPubMed
Moreno-Briseno, P., Diaz, R., Campos-Romo, A., & Fernandez-Ruiz, J. (2010). Sex-related differences in motor learning and performance. Behavioral and Brain Functions, 6(1), 74. doi: 10.1186/1744-9081-6-74CrossRefGoogle ScholarPubMed
Nelson, M. D., Saykin, A. J., Flashman, L. A., & Riordan, H. J. (1998). Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: A meta-analytic study. Archives of General Psychiatry, 55(5), 433440.CrossRefGoogle ScholarPubMed
Pajonk, F. G., Wobrock, T., Gruber, O., Scherk, H., Berner, D., Kaizl, I., … Falkai, P. (2010). Hippocampal plasticity in response to exercise in schizophrenia. Archives of General Psychiatry, 67(2), 133143. doi: 10.1001/archgenpsychiatry.2009.193CrossRefGoogle ScholarPubMed
Palmese, L. B., DeGeorge, P. C., Ratliff, J. C., Srihari, V. H., Wexler, B. E., Krystal, A. D., & Tek, C. (2011). Insomnia is frequent in schizophrenia and associated with night eating and obesity. Schizophrenia Research, 133(1–3), 238243. doi: 10.1016/j.schres.2011.07.030CrossRefGoogle ScholarPubMed
Passos, G. S., Poyares, D., Santana, M. G., Teixeira, A. A., Lira, F. S., Youngstedt, S. D., … de Mello, M. T. (2014). Exercise improves immune function, antidepressive response, and sleep quality in patients with chronic primary insomnia. BioMed Research International, 2014, 498961. doi: 10.1155/2014/498961CrossRefGoogle ScholarPubMed
Penhune, V. B., & Steele, C. J. (2012). Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behavioural Brain Research, 226(2), 579591. doi: 10.1016/j.bbr.2011.09.044CrossRefGoogle ScholarPubMed
Pohlack, S. T., Meyer, P., Cacciaglia, R., Liebscher, C., Ridder, S., & Flor, H. (2014). Bigger is better! Hippocampal volume and declarative memory performance in healthy young men. Brain Structure and Function, 219(1), 255267. doi: 10.1007/s00429-012-0497-zCrossRefGoogle ScholarPubMed
Prince, T. M., & Abel, T. (2013). The impact of sleep loss on hippocampal function. Learning & Memory, 20(10), 558569. doi: 10.1101/lm.031674.113CrossRefGoogle ScholarPubMed
Roig, M., Skriver, K., Lundbye-Jensen, J., Kiens, B., & Nielsen, J. B. (2012). A single bout of exercise improves motor memory. PLoS One, 7(9), e44594. doi: 10.1371/journal.pone.0044594CrossRefGoogle ScholarPubMed
Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klosch, G., Anderer, P., … Zeitlhofer, J. (2004). Sleep spindles and their significance for declarative memory consolidation. Sleep, 27(8), 14791485. doi: 10.1093/sleep/27.7.1479CrossRefGoogle ScholarPubMed
Schacter, D. L., & Tuvling, E. (1995). Memory system 1994. Cambridge, MA: The MIT Press.Google Scholar
Schendan, H. E., Searl, M. M., Melrose, R. J., & Stern, C. E. (2003). An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37(6), 10131025.CrossRefGoogle ScholarPubMed
Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 20(1), 1121.CrossRefGoogle ScholarPubMed
Sirota, A., Csicsvari, J., Buhl, D., & Buzsaki, G. (2003). Communication between neocortex and hippocampus during sleep in rodents. Proceedings of the National Academy of Sciences of the United States of America, 100(4), 20652069. doi: 10.1073/pnas.0437938100CrossRefGoogle ScholarPubMed
Squire, L. R., & Knowlton, B. J. (1994). In the cognitive neurosciences. Cambridge, MA: The MIT Press.Google Scholar
Squire, L. R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science (New York, N.Y.), 253(5026), 13801386.CrossRefGoogle ScholarPubMed
Stendardi, L., Grazzini, M., Gigliotti, F., Lotti, P., & Scano, G. (2005). Dyspnea and leg effort during exercise. Respiratory Medicine, 99(8), 933942. doi: 10.1016/j.rmed.2005.02.005CrossRefGoogle ScholarPubMed
Suzuki, W. A., & Eichenbaum, H. (2000). The neurophysiology of memory. Annals of the New York Academy of Sciences, 911, 175191.CrossRefGoogle ScholarPubMed
Ullman, M. T. (2004). Contributions of memory circuits to language: The declarative/procedural model. Cognition, 92(1–2), 231270. doi: 10.1016/j.cognition.2003.10.008CrossRefGoogle ScholarPubMed
Ungerleider, L. G., Doyon, J., & Karni, A. (2002). Imaging brain plasticity during motor skill learning. Neurobiology of Learning and Memory, 78(3), 553564.CrossRefGoogle ScholarPubMed
Wamsley, E. J., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S. K., Ely, A. V., … Manoach, D. S. (2012). Reduced sleep spindles and spindle coherence in schizophrenia: Mechanisms of impaired memory consolidation? Biological Psychiatry, 71(2), 154161. doi: 10.1016/j.biopsych.2011.08.008CrossRefGoogle ScholarPubMed
Weiss, E. M., Deisenhammer, E. A., Hinterhuber, H., & Marksteiner, J. (2005). Gender differences in cognitive functions. Fortschritte der Neurologie-Psychiatrie, 73(10), 587595. doi: doi:10.1055/s-2004-830296CrossRefGoogle ScholarPubMed
Weiss, E. M., Kemmler, G., Deisenhammer, E. A., Fleischhacker, W. W., & Delazer, M. (2003). Sex differences in cognitive functions. Personality and Individual Differences, 35(4), 863875.CrossRefGoogle Scholar