Motor Adaptation Impairment in Chronic Cannabis Users Assessed by a Visuomotor Rotation Task
Abstract
1. Introduction
2. Experimental Section
2.1. Design
2.2. Participants
2.3. Procedures
2.4. Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- UNODC. World Drug Report. 2016. Available online: https://www.unodc.org/wdr2016/ (accessed on 16 July 2019).
- Al-Imam, A. The Most Popular Chemical Categories of NPS in Four Leading Countries of the Developed World: An Integrative Analysis of Trends Databases, Surface Web, and the Deep Web. Glob. J. Health Sci. 2017, 9, 40. [Google Scholar] [CrossRef][Green Version]
- Koziol, L.F.; Budding, D.; Andreasen, N.; Darrigo, S.; Bulgheroni, S.; Imamizu, H.; Ito, M.; Manto, M.; Marvel, C.; Parker, K.; et al. Consensus Paper: The Cerebellum’s Role in Movement and Cognition. Cerebellum 2014, 13, 151–177. [Google Scholar] [CrossRef] [PubMed]
- Miquel, M.; Vazquez-Sanroman, D.; Carbo-Gas, M.; Gil-Miravet, I.; Sanchis-Segura, C.; Carulli, D.; Manzo, J.; Coria-Avila, G.A. Have we been ignoring the elephant in the room? Seven arguments for considering the cerebellum as part of addiction circuitry. Neurosci. Biol. Rev. 2016, 60, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Hasin, D.S.; Sarvet, A.L.; Cerdá, M.; Keyes, K.M.; Stohl, M.; Galea, S.; Wall, M.M. US Adult Illicit Cannabis Use, Cannabis Use Disorder, and Medical Marijuana Laws1991–1992 to 2012–2013. JAMA Psychiatry 2017, 74, 579–588. [Google Scholar] [CrossRef] [PubMed]
- Hall, W.; Weier, M. Assessing the Public Health Impacts of Legalizing Recreational Cannabis Use in the USA. Clin. Pharmacol. Ther. 2015, 97, 607–615. [Google Scholar] [CrossRef] [PubMed]
- Volkow, N.D.; Swanson, J.M.; Evins, A.E.; DeLisi, L.E.; Meier, M.H.; Gonzalez, R.; Bloomfield, M.A.P.; Curran, H.V.; Baler, R. Effects of cannabis use on human behavior, including cognition, motivation, and psychosis: A review. JAMA Psychiatry 2016, 73, 292–297. [Google Scholar] [CrossRef] [PubMed]
- Crane, N.A.; Schuster, R.M.; Fusar-Poli, P.; Gonzalez, R. Effects of cannabis on neurocognitive functioning: Recent advances, neurodevelopmental influences, and sex differences. Neuropsychol. Rev. 2013, 23, 117–137. [Google Scholar] [CrossRef]
- Ramaekers, J.; Kauert, G.; Theunissen, E.; Toennes, S.; Moeller, M. Neurocognitive performance during acute THC intoxication in heavy and occasional cannabis users. J. Psychopharmacol. 2009, 23, 266–277. [Google Scholar] [CrossRef]
- Meier, M.H.; Caspi, A.; Ambler, A.; Harrington, H.; Houts, R.; Keefe, R.S.E.; McDonald, K.; Ward, A.; Poulton, R.; Moffitt, T.E. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc. Natl. Acad. Sci. USA. 2012, 109, E2657–E2664. [Google Scholar] [CrossRef]
- Prashad, S.; Filbey, F.M. Cognitive motor deficits in cannabis users. Curr. Opin. Behav. Sci. 2017, 13, 1–7. [Google Scholar] [CrossRef]
- Ramaekers, J.G.; Kauert, G.; van Ruitenbeek, P.; Theunissen, E.L.; Schneider, E.; Moeller, M.R. High-Potency Marijuana Impairs Executive Function and Inhibitory Motor Control. Neuropsychopharmacology 2006, 31, 2296–2303. [Google Scholar] [CrossRef] [PubMed]
- Hall, W. What has research over the past two decades revealed about the adverse health effects of recreational cannabis use? Addiction 2015, 110, 19–35. [Google Scholar] [CrossRef] [PubMed]
- Gaoni, Y.; Mechoulam, R. Isolation, structure, and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 1964, 86, 1646–1647. [Google Scholar] [CrossRef]
- Matsuda, L.; Lolait, S.; Brownstein, M.; Young, A.; Bonner, T. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346, 561–564. [Google Scholar] [CrossRef] [PubMed]
- Devane, W.A.; Dysarz, F.A.; Johnson, M.R.; Melvin, L.S.; Howlett, A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 1988, 34, 605–613. [Google Scholar] [PubMed]
- Kano, M.; Ohno-Shosaku, T.; Hashimotodani, Y.; Uchigashima, M.; Watanabe, M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 2009, 89, 309–380. [Google Scholar] [CrossRef] [PubMed]
- Cadogan, A.K.; Alexander, S.P.; Boyd, E.A.; Kendall, D.A. Influence of cannabinoids on electrically evoked dopamine release and cyclic AMP generation in the rat striatum. J. Neurochem. 1997, 69, 1131–1137. [Google Scholar] [CrossRef] [PubMed]
- Tsou, K.; Brown, S.; Sañudo-Peña, M.; Mackie, K.; Walker, J. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 1998, 83, 393–411. [Google Scholar] [CrossRef]
- Egertova, M.; Elphick, M.R. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB1. J. Comp. Neurol. 2000, 422, 159–171. [Google Scholar] [CrossRef]
- Cutando, L.; Busquets-Garcia, A.; Puighermanal, E.; Gomis-González, M.; Delgado-García, J.M.; Gruart, A.; Maldonado, R.; Ozaita, A. Microglial activation underlies cerebellar deficits produced by repeated cannabis exposure. J. Clin. Investig. 2013, 123, 2816–2831. [Google Scholar] [CrossRef]
- Safo, P.K.; Regehr, W.G. Endocannabinoids control the induction of cerebellar LTD. Neuron 2005, 48, 647–659. [Google Scholar] [CrossRef] [PubMed]
- Hesslow, G.; Yeo, C.H. The functional anatomy of skeletal conditioning. In A Neuroscientist’s Guide to Classical Conditioning; Springer: Berlin, Germany, 2002; pp. 86–146. [Google Scholar]
- Kishimoto, Y. Endogenous Cannabinoid Signaling through the CB1 Receptor Is Essential for Cerebellum-Dependent Discrete Motor Learning. J. Neurosci. 2006, 26, 8829–8837. [Google Scholar] [CrossRef] [PubMed]
- Skosnik, P.D.; Edwards, C.R.; O’Donnell, B.F.; Steffen, A.; Steinmetz, J.E.; Hetrick, W.P. Cannabis use disrupts eyeblink conditioning: Evidence for cannabinoid modulation of cerebellar-dependent learning. Neuropsychopharmacology 2008, 33, 1432–1440. [Google Scholar] [CrossRef] [PubMed]
- Shadmehr, R.; Smith, M.A.; Krakauer, J.W. Error correction, sensory prediction, and adaptation in motor control. Annu. Rev. Neurosci. 2010, 33, 89–108. [Google Scholar] [CrossRef] [PubMed]
- Herreros, I.; Verschure, P.F.M.J. Nucleo-olivary inhibition balances the interaction between the reactive and adaptive layers in motor control. Neural Netw. 2013, 47, 64–71. [Google Scholar] [CrossRef] [PubMed]
- Krakauer, J.W.; Pine, Z.M.; Ghilardi, M.F.; Ghez, C. Learning of visuomotor transformations for vectorial planning of reaching trajectories. J. Neurosci. 2000, 20, 8916–8924. [Google Scholar] [CrossRef] [PubMed]
- Mazzoni, P.; Krakauer, J.W. An Implicit Plan Overrides an Explicit Strategy during Visuomotor Adaptation. J. Neurosci. 2006, 26, 3642–3645. [Google Scholar] [CrossRef] [PubMed]
- Weiner, M.J.; Hallett, M.; Funkenstein, H.H. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology 1983, 33, 766–772. [Google Scholar] [CrossRef] [PubMed]
- Schlerf, J.E.; Xu, J.; Klemfuss, N.M.; Griffiths, T.L.; Ivry, R.B. Individuals with cerebellar degeneration show similar adaptation deficits with large and small visuomotor errors. J. Neurophysiol. 2013, 109, 1164–1173. [Google Scholar] [CrossRef]
- Taylor, J.A.; Klemfuss, N.M.; Ivry, R.B. An explicit strategy prevails when the cerebellum fails to compute movement errors. Cerebellum 2010, 9, 580–586. [Google Scholar] [CrossRef]
- Bonn-Miller, M.O.; Heinz, A.J.; Smith, E.V.; Bruno, R.; Adamson, S. Preliminary Development of a Brief Cannabis Use Disorder Screening Tool: The Cannabis Use Disorder Identification Test Short-Form. Cannabis Cannabinoid Res. 2016, 1, 252–261. [Google Scholar] [CrossRef] [PubMed]
- Casajuana, C.; Balcells-Olivero, M.M.; López-Pelayo, H.; Miquel, L.; Teixidó, L.; Colom, J.; Nutt, D.J.; Rehm, J.; Gual, A. The Standard Joint Unit. Drug Alcohol Depend. 2017, 1, 109–116. [Google Scholar] [CrossRef] [PubMed]
- Weyer, A.; Abele, M.; Schmitz-Hübsch, T.; Schoch, B.; Frings, M.; Timmann, D.; Klockgether, T. Reliability and validity of the scale for the assessment and rating of ataxia: A study in 64 ataxia patients. Mov. Disord. 2007, 22, 1633–1637. [Google Scholar] [CrossRef] [PubMed]
- Crean, R.D.; Crane, N.A.; Mason, B.J. An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. J. Addict. Med. 2011, 5, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Taylor, J.A.; Ivry, R.B. Flexible cognitive strategies during motor learning. PLoS Comput. Biol. 2011, 7, e1001096. [Google Scholar] [CrossRef] [PubMed]
- Taylor, J.A.; Krakauer, J.W.; Ivry, R.B. Explicit and implicit contributions to learning in a sensorimotor adaptation task. J. Neurosci. 2014, 34, 3023–3032. [Google Scholar] [CrossRef] [PubMed]
- Beason-Held, L.L.; Goh, J.O.; An, Y.; Kraut, M.A.; O’Brien, R.J.; Ferrucci, L.; Resnick, S.M. Changes in brain function occur years before the onset of cognitive impairment. J. Neurosci. 2013, 33, 18008–18014. [Google Scholar] [CrossRef]
- Nakamura, A.; Cuesta, P.; Kato, T.; Arahata, Y.; Iwata, K.; Yamagishi, M.; Kuratsubo, I.; Kato, K.; Bundo, M.; Diers, K.; et al. Early functional network alterations in asymptomatic elders at risk for Alzheimer’s disease. Sci. Rep. 2017, 7, 6517. [Google Scholar] [CrossRef]
- Nestoros, J.N.; Vakonaki, E.; Tzatzarakis, M.N.; Alegakis, A.; Skondras, M.D.; Tsatsakis, A.M. Long lasting effects of chronic heavy cannabis abuse. Am. J. Addict. 2017, 26, 335–342. [Google Scholar] [CrossRef]
- Blithikioti, C.; Miquel, L.; Batalla, A.; Rubio, B.; Maffei, G.; Herreros, I.; Gual, A.; Verschure, P.; Balcells-Oliveró, M. Cerebellar alterations in cannabis users: A systematic review. Addict. Biol. 2019. [Google Scholar] [CrossRef]
- Morehead, J.R.; Taylor, J.A.; Parvin, D.E.; Ivry, R.B. Characteristics of Implicit Sensorimotor Adaptation Revealed by Task-irrelevant Clamped Feedback. J. Cogn. Neurosci. 2017, 29, 1061–1074. [Google Scholar] [CrossRef] [PubMed]
Experimental (n = 11) | Control (n = 17) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
n | % | Mean | SD | n | % | Mean | SD | χ2/t/fisher | p-Value | |
Men | 7 | 63.6 | 9 | 52.9 | 0.3 | 0.6 | ||||
Age | 28.3 | 8.1 | 30.7 | 7.1 | −0.8 | 0.41 | ||||
Academic Level | 13.7 | <0.001 | ||||||||
High school | 8 | 72.7 | 1 | 5.9 | ||||||
University | 3 | 27.3 | 16 | 94.1 | ||||||
Civil Status | 0.05 | 0.8 | ||||||||
Single | 8 | 72.7 | 13 | 76.5 | ||||||
Married | 3 | 27.3 | 4 | 23.5 | ||||||
Age at first cannabis consumption | 16.6 | 3 | 15 | 2 | ||||||
Age at regular cannabis use | 19 | 2.1 | ||||||||
Regular cigarette smokers (yes) | 4 | 36.4 | 1 | 6.3 | 0.134 | 0.07 | ||||
Frequency of Cannabis use last 6 months | ||||||||||
4 to 6 times per week | 2 | 18.2 | ||||||||
Daily | 9 | 75.0 | ||||||||
SJU/day last 6 months | 3.7 | 3.7 | ||||||||
Frequency of Cannabis use last week | ||||||||||
Never | 2 | 18.2 | ||||||||
2 to 3 times per week | 1 | 69.1 | ||||||||
4 to 6 times per week | 2 | 18.2 | ||||||||
Daily | 6 | 54.5 | ||||||||
SJU/day last week | 2 | 2.2 | ||||||||
Standard drink units per week | 6.7 | 8.3 | 2.9 | 3.9 | 1.6 | 0.1 | ||||
SARA | 0 | 0 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Herreros, I.; Miquel, L.; Blithikioti, C.; Nuño, L.; Rubio Ballester, B.; Grechuta, K.; Gual, A.; Balcells-Oliveró, M.; Verschure, P. Motor Adaptation Impairment in Chronic Cannabis Users Assessed by a Visuomotor Rotation Task. J. Clin. Med. 2019, 8, 1049. https://doi.org/10.3390/jcm8071049
Herreros I, Miquel L, Blithikioti C, Nuño L, Rubio Ballester B, Grechuta K, Gual A, Balcells-Oliveró M, Verschure P. Motor Adaptation Impairment in Chronic Cannabis Users Assessed by a Visuomotor Rotation Task. Journal of Clinical Medicine. 2019; 8(7):1049. https://doi.org/10.3390/jcm8071049
Chicago/Turabian StyleHerreros, Ivan, Laia Miquel, Chrysanthi Blithikioti, Laura Nuño, Belen Rubio Ballester, Klaudia Grechuta, Antoni Gual, Mercè Balcells-Oliveró, and Paul Verschure. 2019. "Motor Adaptation Impairment in Chronic Cannabis Users Assessed by a Visuomotor Rotation Task" Journal of Clinical Medicine 8, no. 7: 1049. https://doi.org/10.3390/jcm8071049
APA StyleHerreros, I., Miquel, L., Blithikioti, C., Nuño, L., Rubio Ballester, B., Grechuta, K., Gual, A., Balcells-Oliveró, M., & Verschure, P. (2019). Motor Adaptation Impairment in Chronic Cannabis Users Assessed by a Visuomotor Rotation Task. Journal of Clinical Medicine, 8(7), 1049. https://doi.org/10.3390/jcm8071049