Similar cognitive deficits in mice and humans in the chronic phase post-stroke identified using the touchscreen-based paired-associate learning task

Article


Chow, Wei Zhen, Ong, Lin Kooi, Kluge, Murielle G., Gyawali, Prajwal, Walker, Frederick R. and Nilsson, Michael. 2020. "Similar cognitive deficits in mice and humans in the chronic phase post-stroke identified using the touchscreen-based paired-associate learning task." Scientific Reports. 10, pp. 1-8. https://doi.org/10.1038/s41598-020-76560-x
Article Title

Similar cognitive deficits in mice and humans in the chronic phase post-stroke identified using the touchscreen-based paired-associate learning task

ERA Journal ID201487
Article CategoryArticle
AuthorsChow, Wei Zhen (Author), Ong, Lin Kooi (Author), Kluge, Murielle G. (Author), Gyawali, Prajwal (Author), Walker, Frederick R. (Author) and Nilsson, Michael (Author)
Journal TitleScientific Reports
Journal Citation10, pp. 1-8
Article Number19545
Number of Pages8
Year2020
PublisherNature Publishing Group
Place of PublicationUnited Kingdom
ISSN2045-2322
Digital Object Identifier (DOI)https://doi.org/10.1038/s41598-020-76560-x
Web Address (URL)https://www.nature.com/articles/s41598-020-76560-x
Abstract

For many chronic stroke survivors, persisting cognitive dysfunction leads to significantly reduced quality of life. Translation of promising therapeutic strategies aimed at improving cognitive function is hampered by existing, disparate cognitive assessments in animals and humans. In this study, we assessed post-stroke cognitive function using a comparable touchscreen-based paired-associate learning task in a cross-sectional population of chronic stroke survivors (≥ 5 months post-stroke, n = 70), age-matched controls (n = 70), and in mice generated from a C57BL/6 mouse photothrombotic stroke model (at six months post-stroke). Cognitive performance of stroke survivors was analysed using linear regression adjusting for age, gender, diabetes, systolic blood pressure and waist circumference. Stroke survivors made significantly fewer correct choices across all tasks compared with controls. Similar cognitive impairment was observed in the mice post-stroke with fewer correct choices compared to shams. These results highlight the feasibility and potential value of analogous modelling of clinically meaningful cognitive impairments in chronic stroke survivors and in mice in chronic phase after stroke. Implementation of validated, parallel cross-species test platforms for cognitive assessment offer the potential of delivering a more useful framework for evaluating therapies aimed at improving long-term cognitive function post-stroke.

Keywordsstroke survivors, PAL Task, cognitive disorders
ANZSRC Field of Research 2020320905. Neurology and neuromuscular diseases
Byline AffiliationsUniversity of Newcastle
School of Health and Wellbeing
Institution of OriginUniversity of Southern Queensland
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Growth Hormone Improves Cognitive Function After Experimental Stroke
Ong, Lin Kooi, Chow, Wei Zhen, TeBay, Clifford, Kluge, Murielle, Pietrogrande, Giovanni, Zalewska, Katarzyna, Crock, Patricia, Åberg, N. David, Bivard, Andrew, Johnson, Sarah J., Walker, Frederick R., Nilsson, Michael and Isgaard, Jorgen. 2018. "Growth Hormone Improves Cognitive Function After Experimental Stroke." Stroke. 49 (5), pp. 1257 - 1266. https://doi.org/10.1161/STROKEAHA.117.020557
Sustained administration of corticosterone at stress-like levels after stroke suppressed glial reactivity at sites of thalamic secondary neurodegeneration
Zalewska, Katarzyna, Pietrogrande, Giovanni, Ong, Lin Kooi, Abdolhoseini, Mahmoud, Kluge, Murielle, Johnson, Sarah J., Walker, Frederick R. and Nilsson, Michael. 2018. "Sustained administration of corticosterone at stress-like levels after stroke suppressed glial reactivity at sites of thalamic secondary neurodegeneration." Brain, Behavior, and Immunity. 69, pp. 210-222. https://doi.org/10.1016/j.bbi.2017.11.014
Physical activity for cognitive and mental health in youth: A systematic review of mechanisms
Lubans, David, Richards, Justin, Hillman, Charles, Faulkner, Guy, Beauchamp, Mark, Nilsson, Michael, Kelly, Paul, Smith, Jordan, Raine, Lauren and Biddle, Stuart. 2016. "Physical activity for cognitive and mental health in youth: A systematic review of mechanisms." Pediatrics. 138 (3), pp. 1-15. https://doi.org/10.1542/peds.2016-1642
Chronic stress induced disruption of the peri-infarct neurovascular unit following experimentally induced photothrombotic stroke
Zhao, Zidan, Ong, Lin Kooi, Johnson, Sarah, Nilsson, Michael and Walker, Frederick R.. 2017. "Chronic stress induced disruption of the peri-infarct neurovascular unit following experimentally induced photothrombotic stroke." Journal of Cerebral Blood Flow and Metabolism. 37 (12), pp. 3709-3724. https://doi.org/10.1177/0271678X17696100
Impaired microglia process dynamics post-stroke are specific to sites of secondary neurodegeneration
Kluge, Murielle G., Kracht, Laura, Mahmoud Abdolhoseini, Ong, Lin Kooi, Johnson, Sarah J., Nilsson, Michael and Walker, Frederick R.. 2017. "Impaired microglia process dynamics post-stroke are specific to sites of secondary neurodegeneration." Glia. 65 (12), pp. 1885-1899. https://doi.org/10.1002/glia.23201
Peripheral Lipopolysaccharide Challenge Induces Long-Term Changes in Tyrosine Hydroxylase Regulation in the Adrenal Medulla
Ong, Lin Kooi, Page, Scott, Briggs, Gabrielle D., Guan, Liying, Dun, Matthew D., Verrills, Nicole M., Dunkley, Peter R. and Dickson, Phillip W.. 2017. "Peripheral Lipopolysaccharide Challenge Induces Long-Term Changes in Tyrosine Hydroxylase Regulation in the Adrenal Medulla." Journal of Cellular Biochemistry. 118 (8), pp. 2096-2107. https://doi.org/10.1002/jcb.25839
Oral administration of corticosterone at stress-like levels drives microglial but not vascular disturbances post-stroke
Zalewska, Katarzyna, Ong, Lin Kooi, Johnson, Sarah J., Nilsson, Michael and Walker, Frederick R.. 2017. "Oral administration of corticosterone at stress-like levels drives microglial but not vascular disturbances post-stroke." Neuroscience. 352, pp. 30-38. https://doi.org/10.1016/j.neuroscience.2017.03.005
Oral corticosterone administration alone is sufficient to simulate the actions of chronic stress on glial cells but not on vasculature
Zalewska, K., Ong, L. K., Pietrogrande, G., Johnson, S. J., Nilsson, M. and Walker, F. R.. 2017. "Oral corticosterone administration alone is sufficient to simulate the actions of chronic stress on glial cells but not on vasculature." 13th European Meeting on Glial Cells in Health and Disease (2017). Scotland 08 - 11 Jul 2017 United States.
Chronic stress exposure following photothrombotic stroke is associated with increased levels of Amyloid beta accumulation and altered oligomerisation at sites of thalamic secondary neurodegeneration in mice
Ong, Lin Kooi, Zhao, Zidan, Kluge, Murielle, Walker, Frederick R. and Nilsson, Michael. 2017. "Chronic stress exposure following photothrombotic stroke is associated with increased levels of Amyloid beta accumulation and altered oligomerisation at sites of thalamic secondary neurodegeneration in mice." Journal of Cerebral Blood Flow and Metabolism. 37 (4), pp. 1338-1348. https://doi.org/10.1177/0271678X16654920
Authors’ response re: ‘‘Reconsidering the role of glial cells in chronic stress-induced dopaminergic neurons loss within the substantia nigra? Friend of foe?” by Ong et al. Brain Behavior and Immunity, 2016
Ong, Lin Kooi, Nilsson, Michael and Walker, Frederick R.. 2017. "Authors’ response re: ‘‘Reconsidering the role of glial cells in chronic stress-induced dopaminergic neurons loss within the substantia nigra? Friend of foe?” by Ong et al. Brain Behavior and Immunity, 2016." Brain, Behavior, and Immunity. 60, pp. 384-384. https://doi.org/10.1016/j.bbi.2016.11.029
Reconsidering the role of glial cells in chronic stress-induced dopaminergic neurons loss within the substantia nigra? Friend or foe?
Ong, Lin Kooi, Zhao, Zidan, Kluge, Murielle, TeBay, Clifford, Zalewska, Katarzyna, Dickson, Phillip W., Johnson, Sarah J., Nilsson, Michael and Walker, Frederick R.. 2017. "Reconsidering the role of glial cells in chronic stress-induced dopaminergic neurons loss within the substantia nigra? Friend or foe?" Brain, Behavior, and Immunity. 60, pp. 117-125. https://doi.org/10.1016/j.bbi.2016.10.001
Early life peripheral lipopolysaccharide challenge reprograms catecholaminergic neurons
Ong, Lin Kooi, Fuller, Erin A., Sominsky, Luba, Hodgson, Deborah M., Dunkley, Peter R. and Dickson, Phillip W.. 2017. "Early life peripheral lipopolysaccharide challenge reprograms catecholaminergic neurons." Scientific Reports. 7, pp. 1-6. https://doi.org/10.1038/srep40475
Rapamycin reduces motivated responding for cocaine and alters GluA1 expression in the ventral but not dorsal striatum
James, Morgan H., Quinn, Rikki K., Ong, Lin Kooi, Levi, Emily M., Smith, Doug W., Dickson, Phillip W. and Dayas, Christopher V.. 2016. "Rapamycin reduces motivated responding for cocaine and alters GluA1 expression in the ventral but not dorsal striatum." European Journal of Pharmacology. 784, pp. 147-154. https://doi.org/10.1016/j.ejphar.2016.05.013
Tyrosine hydroxylase regulation in adult rat striatum following short-term neonatal exposure to manganese
Peres, Tanara V., Ong, Lin K., Costa, Ana Paula, Eyng, Helena, Venske, De´bora K. R., Colle, Dirleise, Gonçalves, Filipe M., Lopes, Mark W., Farina, Marcelo, Aschner, Michael, Dickson, Phillip W., Dunkley, Peter R. and Leal, Rodrigo B.. 2016. "Tyrosine hydroxylase regulation in adult rat striatum following short-term neonatal exposure to manganese." Metallomics: integrated biometal science. 8 (6), pp. 597-604. https://doi.org/10.1039/c5mt00265f
Inflammation and dopamine synthesis in neurodegeneration
Ong, Lin Kooi, Briggs, G., Guan, L., Dunkley, P. and Dickson, P.. 2015. "Inflammation and dopamine synthesis in neurodegeneration." 25th Biennial Meeting of the International-Society-for-Neurochemistry Jointly with the 13th Meeting of the Asian-Pacific-Society-for-Neurochemistry in Conjunction with the 35th Meeting of the Australasian-Neuroscience-Society (2015). Cairns, Australia 23 - 27 Aug 2015 United Kingdom.
Hemorheology, ankle brachial pressure index (ABPI) and toe brachial pressure index (TBPI) in metabolic syndrome
Gyawali, Prajwal, Richards, Ross S., Tinley, Paul and Nwose, Ezekiel Uba. 2014. "Hemorheology, ankle brachial pressure index (ABPI) and toe brachial pressure index (TBPI) in metabolic syndrome ." Microvascular Research. 95, pp. 31-36. https://doi.org/10.1016/j.mvr.2014.06.013
The role of inflammation and dopamine synthesis in Parkinson's disease
Ong, L. K., Briggs, G. D., Dunkley, P. R. and Dickson, P. W.. 2014. "The role of inflammation and dopamine synthesis in Parkinson's disease." 12th Biennial Meeting of the Asian-Pacific-Society-for-Neurochemistry (2014). Taiwan 23 - 26 Aug 2014 United Kingdom.
mTORC1 Inhibition in the Nucleus Accumbens ‘Protects’ Against the Expression of Drug Seeking and ‘Relapse’ and Is Associated with Reductions in GluA1 AMPAR and CAMKIIa Levels
James, Morgan H., Quinn, Rikki K., Ong, Lin Kooi, Levi, Emily M., Charnley, Janine L., Smith, Doug W., Dickson, Phillip W. and Dayas, Christopher V.. 2014. "mTORC1 Inhibition in the Nucleus Accumbens ‘Protects’ Against the Expression of Drug Seeking and ‘Relapse’ and Is Associated with Reductions in GluA1 AMPAR and CAMKIIa Levels." Neuropsychopharmacology. 39 (7), pp. 1694-1702. https://doi.org/10.1038/npp.2014.16
Neurobiological consequences of acute footshock stress: effects on tyrosine hydroxylase phosphorylation and activation in the rat brain and adrenal medulla
Ong, Lin Kooi, Guan, Liying, Damanhuri, Hanafi, Goodchild, Ann K., Bobrovskaya, Larisa, Dickson, Phillip W. and Dunkley, Peter R.. 2014. "Neurobiological consequences of acute footshock stress: effects on tyrosine hydroxylase phosphorylation and activation in the rat brain and adrenal medulla." Journal of Neurochemistry. 128 (4), pp. 547-560. https://doi.org/10.1111/jnc.12482
Product of serum calcium and phosphorus (Ca× PO4) as predictor of cardiovascular disease risk in predialysis patients
Regmi, Prashant, Malla, Bimala, Gyawali, Prajwal, Sigdel, Manoj, Shrestha, Rojeet, Shah, Dibya Singh and Khanal, Madhav Prasad. 2014. "Product of serum calcium and phosphorus (Ca× PO4) as predictor of cardiovascular disease risk in predialysis patients." Clinical Biochemistry. 47 (1-2), pp. 77-81. https://doi.org/10.1016/j.clinbiochem.2013.09.012
Erythrocyte aggregation and metabolic syndrome
Gyawali, Prajwal, Richards, Ross S., Hughes, Diane L. and Tinley, Paul. 2014. "Erythrocyte aggregation and metabolic syndrome." Clinical Hemorheology and Microcirculation. 57 (1), pp. 73-83. https://doi.org/10.3233/CH-131792
Early Life Stress and Post-Weaning High Fat Diet Alter Tyrosine Hydroxylase Regulation and AT1 Receptor Expression in the Adrenal Gland in a Sex Dependent Manner
Bobrovskaya, Larisa, Maniam, Jayanthi, Ong, Lin Kooi, Dunkley, Peter R. and Morris, Margaret J.. 2013. "Early Life Stress and Post-Weaning High Fat Diet Alter Tyrosine Hydroxylase Regulation and AT1 Receptor Expression in the Adrenal Gland in a Sex Dependent Manner." Neurochemical Research. 38 (4), pp. 826-833. https://doi.org/10.1007/s11064-013-0985-4
Functional Programming of the Autonomic Nervous System by Early Life Immune Exposure: Implications for Anxiety
Sominsky, Luba, Fuller, Erin A., Bondarenko, Evgeny, Ong, Lin Kooi, Averell, Lee, Nalivaiko, Eugene, Dunkley, Peter R., Dickson, Phillip W. and Hodgson, Deborah M.. 2013. "Functional Programming of the Autonomic Nervous System by Early Life Immune Exposure: Implications for Anxiety." PLoS One. 8 (3), pp. 1-13. https://doi.org/10.1371/journal.pone.0057700
Whole-blood viscosity and metabolic syndrome
Gyawali, Prajwal, Richards, Ross S, Nwose, Ezekiel Uba and Bwititi, Phillip T. 2012. "Whole-blood viscosity and metabolic syndrome ." Clinical Lipidology. 7 (6), pp. 709-719. https://doi.org/10.2217/CLP.12.65
Tyrosine Hydroxylase Phosphorylation in Catecholaminergic Brain Regions: A Marker of Activation following Acute Hypotension and Glucoprivation
Damanhuri, Hanafi A., Burke, Peter G. R., Ong, Lin K., Bobrovskaya, Larisa, Dickson, Phillip W., Dunkley, Peter R. and Goodchild, Ann K.. 2012. "Tyrosine Hydroxylase Phosphorylation in Catecholaminergic Brain Regions: A Marker of Activation following Acute Hypotension and Glucoprivation." PLoS One. 7 (11), pp. 1-19. https://doi.org/10.1371/journal.pone.0050535
Erythrocyte morphology in metabolic syndrome
Gyawali, Prajwal, Richards, Ross S. and Nwose, Ezekiel Uba. 2012. "Erythrocyte morphology in metabolic syndrome ." Expert Review of Hematology. 5 (5), pp. 523-531. https://doi.org/10.1586/EHM.12.47
The Sustained Phase of Tyrosine Hydroxylase Activation In vivo
Ong, Lin Kooi, Sominsky, Luba, Dickson, Phillip W., Hodgson, Deborah M. and Dunkley, Peter R.. 2012. "The Sustained Phase of Tyrosine Hydroxylase Activation In vivo." Neurochemical Research. 37 (9), pp. 1938-1943. https://doi.org/10.1007/s11064-012-0812-3
Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic
Sominsky, L., Walker, A. K., Ong, L. K., Tynan, R. J., Walker, F. R. and Hodgson, D. M.. 2012. "Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic." Behavioural Brain Research. 226 (1), pp. 351-356. https://doi.org/10.1016/j.bbr.2011.08.038
The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland
Ong, L. K., Guan, L., Stutz, B., Dickson, P. W., Dunkley, P. R. and Bobrovskaya, L.. 2011. "The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland." Neuroscience. 192, pp. 20-27. https://doi.org/10.1016/j.neuroscience.2011.06.087
Epigenetic Inheritance of Anxiety-Like Behaviour in Rats - Role of Early Life Exposure to a Bacterial Mimetic
Sominsky, L., Walker, A. K., Ong, L., Tynan, R. J., Walker, F. R. and Hodgson, D. M.. 2011. "Epigenetic Inheritance of Anxiety-Like Behaviour in Rats - Role of Early Life Exposure to a Bacterial Mimetic." Journal of Developmental Origins of Health and Disease. 2, pp. S109-S109.
Neonatal respiratory infection and adult re-infection: Effect on glucocorticoid and mineralocorticoid receptors in the hippocampus in BALB/c mice
Wynne, O., Horvat, J. C., Kim, R. Y., Ong, L. K., Smith, R., Hansbro, P. M., Clifton, V. L. and Hodgson, D. M.. 2011. "Neonatal respiratory infection and adult re-infection: Effect on glucocorticoid and mineralocorticoid receptors in the hippocampus in BALB/c mice." Brain, Behavior, and Immunity. 25 (6), pp. 1214-1222. https://doi.org/10.1016/j.bbi.2011.03.014
Sustained Phosphorylation of Tyrosine Hydroxylase at Serine 40 in VIVO
Ong, L. K., Sominsky, L., Walker, A. K., Hodgson, D. M., Goodchild, A. K., Bobrovskaya, L., Dickson, P. W. and Dunkley, P. R.. 2011. "Sustained Phosphorylation of Tyrosine Hydroxylase at Serine 40 in VIVO." 23rd Biennial Meeting of the International Society for Neurochemistry (2011). Athen, Greece 28 Aug - 01 Sep 2011 United Kingdom.
The Effect of Social Defeat on Tyrosine Hydroxylase Phosphorylation in the Rat Brain and Adrenal Gland
Ong, Lin Kooi, Bobrovskaya, Larisa, Walker, Frederick R., Day, Trevor A., Dickson, Phillip W. and Dunkley, Peter R.. 2011. "The Effect of Social Defeat on Tyrosine Hydroxylase Phosphorylation in the Rat Brain and Adrenal Gland." Neurochemical Research. 36 (1), pp. 27-33. https://doi.org/10.1007/s11064-010-0255-7
Tyrosine hydroxylase phosphorylation in response to footshock and restraint stress
Ong, L., Guan, L., Stutz, B., Dickson, P., Dunkley, P. and Bobrovskaya, L.. 2010. "Tyrosine hydroxylase phosphorylation in response to footshock and restraint stress." Journal of Neurochemistry. 115, pp. 77-77.
Signal transduction pathways and tyrosine hydroxylase regulation in the adrenal medulla following glucoprivation: An in vivo analysis
Bobrovskaya, Larisa, Damanhuri, Hanafi A., Ong, Lin Kooi, Schneider, Jennifer J., Dickson, Phillip W., Dunkley, Peter R. and Goodchild, Ann K.. 2010. "Signal transduction pathways and tyrosine hydroxylase regulation in the adrenal medulla following glucoprivation: An in vivo analysis." Neurochemistry International: the journal for the publication of cellular and molecular aspects of neurochemistry. 57 (2), pp. 162-167. https://doi.org/10.1016/j.neuint.2010.05.009
The effect of social conflict on tyrosine hydroxylase phosphorylation in catecholamine-producing cells from sprague-dawley rats
Ong, L., Bobrovskaya, L., Walker, F., Day, Trevor, Dickson, P. and Dunkley, P.. 2009. "The effect of social conflict on tyrosine hydroxylase phosphorylation in catecholamine-producing cells from sprague-dawley rats." 22nd Biennial Meeting of the International Society for Neurochemistry & Asian Pacific Society for Neurochemistry (2009). South Korea 23 - 29 Aug 2009 United Kingdom.
Cross-neutralisation of Australian brown and tiger snake venoms with commercial antivenoms: Cross-reactivity or antivenom mixtures?
O’Leary, Margaret A., Schneider, Jennifer J., Prakash Krishnan, Brian, Lavis, Christopher, McKendry, Amy, Ong, Lin Kooi and Isbister, Geoffrey K.. 2007. "Cross-neutralisation of Australian brown and tiger snake venoms with commercial antivenoms: Cross-reactivity or antivenom mixtures?" Toxicon. 50 (2), pp. 206-213. https://doi.org/10.1016/j.toxicon.2007.03.014