Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T11:08:05.574Z Has data issue: false hasContentIssue false

Regular recreational Cannabis users exhibit altered neural oscillatory dynamics during attention reorientation

Published online by Cambridge University Press:  22 September 2021

Seth D. Springer
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
Rachel K. Spooner
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
Mikki Schantell
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
Yasra Arif
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
Michaela R. Frenzel
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
Jacob A. Eastman
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
Tony W. Wilson*
Affiliation:
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA
*
Author for correspondence: Tony W. Wilson, E-mail: tony.wilson@boystown.org

Abstract

Background

Cannabis is the most widely used illicit drug in the United States and is often associated with changes in attention function, which may ultimately impact numerous other cognitive faculties (e.g. memory, executive function). Importantly, despite the increasing rates of cannabis use and widespread legalization in the United States, the neural mechanisms underlying attentional dysfunction in chronic users are poorly understood.

Methods

We used magnetoencephalography (MEG) and a modified Posner cueing task in 21 regular cannabis users and 32 demographically matched non-user controls. MEG data were imaged in the time−frequency domain using a beamformer and peak voxel time series were extracted to quantify the oscillatory dynamics underlying use-related aberrations in attentional reorienting, as well as the impact on spontaneous neural activity immediately preceding stimulus onset.

Results

Behavioral performance on the task (e.g. reaction time) was similar between regular cannabis users and non-user controls. However, the neural data indicated robust theta-band synchronizations across a distributed network during attentional reorienting, with activity in the bilateral inferior frontal gyri being markedly stronger in users relative to controls (p's < 0.036). Additionally, we observed significantly reduced spontaneous theta activity across this distributed network during the pre-stimulus baseline in cannabis users relative to controls (p's < 0.020).

Conclusions

Despite similar performance on the task, we observed specific alterations in the neural dynamics serving attentional reorienting in regular cannabis users compared to controls. These data suggest that regular cannabis users may employ compensatory processing in the prefrontal cortices to efficiently reorient their attention relative to non-user controls.

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

Arif, Y., Spooner, R. K., Wiesman, A. I., Embury, C. M., Proskovec, A. L., & Wilson, T. W. (2020a). Modulation of attention networks serving reorientation in healthy aging. Aging, 12(13), 1258212597. 10.18632/aging.103515.CrossRefGoogle ScholarPubMed
Arif, Y., Wiesman, A. I., O'Neill, J., Embury, C., May, P. E., Lew, B. J., … Wilson, T. W. (2020b). The age-related trajectory of visual attention neural function is altered in adults living with HIV: A cross-sectional MEG study. EBioMedicine, 61, 103065. doi: 10.1016/j.ebiom.2020.103065CrossRefGoogle ScholarPubMed
Azofeifa, A., Mattson, M. E., Schauer, G., McAfee, T., Grant, A., & Lyerla, R. (2016). National estimates of marijuana use and related indicators — national survey on drug use and health, United States, 2002–2014. MMWR. Surveillance Summaries, 65(11), 128. doi: 10.15585/mmwr.ss6511a1CrossRefGoogle Scholar
Block, R. I., O'Leary, D. S., Ehrhardt, J. C., Augustinack, J. C., Ghoneim, M. M., Arndt, S., & Hall, J. A. (2000). Effects of frequent marijuana use on brain tissue volume and composition. Neuroreport, 11(3), 491496. doi: 10.1097/00001756-200002280-00013CrossRefGoogle ScholarPubMed
Bloomfield, M. A. P., Hindocha, C., Green, S. F., Wall, M. B., Lees, R., Petrilli, K., … Freeman, T. P. (2019). The neuropsychopharmacology of cannabis: A review of human imaging studies. Pharmacology & Therapeutics, 195, 132161. doi: 10.1016/j.pharmthera.2018.10.006CrossRefGoogle ScholarPubMed
Böcker, K. B., Hunault, C. C., Gerritsen, J., Kruidenier, M., Mensinga, T. T., & Kenemans, J. L. (2010). Cannabinoid modulations of resting state EEG θ power and working memory are correlated in humans. Journal of Cognitive Neuroscience, 22(9), 19061916. doi: 10.1162/jocn.2009.21355CrossRefGoogle ScholarPubMed
Bonnet, U., & Preuss, U. (2017). The cannabis withdrawal syndrome: Current insights. Substance Abuse and Rehabilitation, 8, 937. doi: 10.2147/sar.s109576CrossRefGoogle ScholarPubMed
Bosker, W. M., Karschner, E. L., Lee, D., Goodwin, R. S., Hirvonen, J., Innis, R. B., … Ramaekers, J. G. (2013). Psychomotor function in chronic daily cannabis smokers during sustained abstinence. PLoS One, 8(1), e53127. doi: 10.1371/journal.pone.0053127CrossRefGoogle ScholarPubMed
Broyd, S. J., van Hell, H. H., Beale, C., Yucel, M., & Solowij, N. (2016). Acute and chronic effects of cannabinoids on human cognition—A systematic review. Biological Psychiatry, 79(7), 557567. doi: 10.1016/j.biopsych.2015.12.002CrossRefGoogle ScholarPubMed
Carliner, H., Brown, Q. L., Sarvet, A. L., & Hasin, D. S. (2017). Cannabis use, attitudes, and legal status in the U.S.: A review. Preventive Medicine, 104, 1323. doi: 10.1016/j.ypmed.2017.07.008CrossRefGoogle ScholarPubMed
Casagrande, CC, Lew, BJ, Taylor, BK, Schantell, M, O'Neill, J, May, PE, … Wilson, TW. (2021). Impact of HIV-infection on human somatosensory processing, spontaneous cortical activity, and cortical thickness: A multimodal neuroimaging approach. . Human Brain Mapping, 42(9), 28512861. doi: 10.1002/hbm.25408.CrossRefGoogle ScholarPubMed
Chang, L. (2006). Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain, 129(5), 10961112. doi:10.1093/brain/awl064.CrossRefGoogle ScholarPubMed
Chica, A. B., Bartolomeo, P., & Lupiáñez, J. (2013). Two cognitive and neural systems for endogenous and exogenous spatial attention. Behavioural Brain Research, 237, 107123. doi:10.1016/j.bbr.2012.09.027.CrossRefGoogle ScholarPubMed
Cohen, K., & Weinstein, A. (2018). The effects of cannabinoids on executive functions: Evidence from Cannabis and synthetic cannabinoids—A systematic review. Brain Sciences, 8(3), 40. doi: 10.3390/brainsci8030040CrossRefGoogle ScholarPubMed
Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain: From environment to theory of mind. Neuron, 58(3), 306324. doi: 10.1016/j.neuron.2008.04.017CrossRefGoogle ScholarPubMed
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201215. doi: 10.1038/nrn755CrossRefGoogle ScholarPubMed
Daitch, A. L., Sharma, M., Roland, J. L., Astafiev, S. V., Bundy, D. T., Gaona, C. M., … Corbetta, M. (2013). Frequency-specific mechanism links human brain networks for spatial attention. Proceedings of the National Academy of Sciences of the United States of America, 110(48), 1958519590. doi: 10.1073/pnas.1307947110CrossRefGoogle ScholarPubMed
Dougherty, D. M., Mathias, C. W., Dawes, M. A., Furr, R. M., Charles, N. E., Liguori, A., … Acheson, A. (2013). Impulsivity, attention, memory, and decision-making among adolescent marijuana users. Psychopharmacology, 226(2), 307319. doi: 10.1007/s00213-012-2908-5CrossRefGoogle ScholarPubMed
Eldreth, D. A., Matochik, J. A., Cadet, J. L., & Bolla, K. I. (2004). Abnormal brain activity in prefrontal brain regions in abstinent marijuana users. Neuroimage, 23(3), 914920. doi:10.1016/j.neuroimage.2004.07.032.CrossRefGoogle ScholarPubMed
Fried, P. A., Watkinson, B., & Gray, R. (2005). Neurocognitive consequences of marihuana—A comparison with pre-drug performance. Neurotoxicology and Teratology, 27(2), 231239. doi: 10.1016/j.ntt.2004.11.003CrossRefGoogle ScholarPubMed
Fries, P. (2015). Rhythms for cognition: Communication through coherence. Neuron, 88(1), 220235. doi: 10.1016/j.neuron.2015.09.034CrossRefGoogle ScholarPubMed
Ganzer, F., Bröning, S., Kraft, S., Sack, P.-M., & Thomasius, R. (2016). Weighing the evidence: A systematic review on long-term neurocognitive effects of cannabis use in abstinent adolescents and adults. Neuropsychology Review, 26(2), 186222. doi: 10.1007/s11065-016-9316-2CrossRefGoogle ScholarPubMed
Gilman, J. M., Yucel, M. A., Pachas, G. N., Potter, K., Levar, N., Broos, H., … Evins, A. E. (2019). Delta-9-tetrahydrocannabinol intoxication is associated with increased prefrontal activation as assessed with functional near-infrared spectroscopy: A report of a potential biomarker of intoxication. Neuroimage, 197, 575585. doi: 10.1016/j.neuroimage.2019.05.012CrossRefGoogle ScholarPubMed
Gross, J., Kujala, J., Hamalainen, M., Timmermann, L., Schnitzler, A., & Salmelin, R. (2001). Dynamic imaging of coherent sources: Studying neural interactions in the human brain. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 694699. doi: 10.1073/pnas.98.2.694CrossRefGoogle ScholarPubMed
Hajos, M., Hoffmann, W. E., & Kocsis, B. (2008). Activation of cannabinoid-1 receptors disrupts sensory gating and neuronal oscillation: Relevance to schizophrenia. Biological Psychiatry, 63(11), 10751083. doi: 10.1016/j.biopsych.2007.12.005CrossRefGoogle ScholarPubMed
Hajos, N., Katona, I., Naiem, S. S., MacKie, K., Ledent, C., Mody, I., & Freund, T. F. (2000). Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. European Journal of Neuroscience, 12(9), 32393249. doi: 10.1046/j.1460-9568.2000.00217.xCrossRefGoogle ScholarPubMed
Hanson, K. L., Winward, J. L., Schweinsburg, A. D., Medina, K. L., Brown, S. A., & Tapert, S. F. (2010). Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addictive Behaviors, 35(11), 970976. doi: 10.1016/j.addbeh.2010.06.012CrossRefGoogle ScholarPubMed
Heinrichs-Graham, E., Arpin, D. J., & Wilson, T. W. (2016). Cue-related temporal factors modulate movement-related beta oscillatory activity in the human motor circuit. Journal of Cognitive Neuroscience, 28(7), 10391051. doi: 10.1162/jocn_a_00948CrossRefGoogle ScholarPubMed
Heinrichs-Graham, E., Kurz, M. J., Gehringer, J. E., & Wilson, T. W. (2017). The functional role of post-movement beta oscillations in motor termination. Brain Structure & Function, 222(7), 30753086. doi: 10.1007/s00429-017-1387-1CrossRefGoogle ScholarPubMed
Heinrichs-Graham, E., & Wilson, T. W. (2015). Coding complexity in the human motor circuit. Human Brain Mapping, 36(12), 51555167. doi: 10.1002/hbm.23000CrossRefGoogle ScholarPubMed
Heinrichs-Graham, E., & Wilson, T. W. (2016). Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging. Neuroimage, 134, 514521. doi: 10.1016/j.neuroimage.2016.04.032CrossRefGoogle ScholarPubMed
Herning, R. I., Better, W., Tate, K., & Cadet, J. L. (2003). EEG Deficits in chronic marijuana abusers during monitored abstinence: Preliminary findings. Annals of the New York Academy of Sciences, 993, 7578, discussion 79-81. doi:10.1111/j.1749-6632.2003.tb07513.x.CrossRefGoogle ScholarPubMed
Hillebrand, A., Singh, K. D., Holliday, I. E., Furlong, P. L., & Barnes, G. R. (2005). A new approach to neuroimaging with magnetoencephalography. Human Brain Mapping, 25(2), 199211. doi: 10.1002/hbm.20102CrossRefGoogle ScholarPubMed
Hooper, S. R., Woolley, D., & De Bellis, M. D. (2014). Intellectual, neurocognitive, and academic achievement in abstinent adolescents with cannabis use disorder. Psychopharmacology, 231(8), 14671477. doi: 10.1007/s00213-014-3463-zCrossRefGoogle ScholarPubMed
Huijbregts, S. C. J., Griffith-Lendering, M. F. H., Vollebergh, W. A. M., & Swaab, H. (2014). Neurocognitive moderation of associations between cannabis use and psychoneuroticism. Journal of Clinical and Experimental Neuropsychology, 36(8), 794805. doi:10.1080/13803395.2014.943694.CrossRefGoogle ScholarPubMed
Ilan, A. B., Smith, M. E., & Gevins, A. (2004). Effects of marijuana on neurophysiological signals of working and episodic memory. Psychopharmacology (Berl), 176(2), 214222. doi: 10.1007/s00213-004-1868-9CrossRefGoogle ScholarPubMed
Jager, G., Kahn, R. S., Van Den Brink, W., Van Ree, J. M., & Ramsey, N. F. (2006). Long-term effects of frequent cannabis use on working memory and attention: An fMRI study. Psychopharmacology, 185(3), 358368. doi:10.1007/s00213-005-0298-7.CrossRefGoogle ScholarPubMed
Jager, G., Van Hell, H. H., De Win, M. M., Kahn, R. S., Van Den Brink, W., Van Ree, J. M., & Ramsey, N. F. (2007). Effects of frequent cannabis use on hippocampal activity during an associative memory task. European Neuropsychopharmacology, 17(4), 289297. doi: 10.1016/j.euroneuro.2006.10.003CrossRefGoogle ScholarPubMed
Kanayama, G., Rogowska, J., Pope, H. G., Gruber, S. A., & Yurgelun-Todd, D. A. (2004). Spatial working memory in heavy cannabis users: A functional magnetic resonance imaging study. Psychopharmacology (Berl), 176(3–4), 239247. doi: 10.1007/s00213-004-1885-8CrossRefGoogle ScholarPubMed
Katona, I., Sperlagh, B., Sik, A., Kafalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. Journal of Neuroscience, 19(11), 45444558. doi: 10.1523/JNEUROSCI.19-11-04544.1999CrossRefGoogle ScholarPubMed
Klimesch, W. (2012). Alpha-band oscillations, attention, and controlled access to stored information. Trends in Cognitive Sciences, 16(12), 606617. doi: 10.1016/j.tics.2012.10.007CrossRefGoogle ScholarPubMed
Kovach, C. K., & Gander, P. E. (2016). The demodulated band transform. Journal of Neuroscience Methods, 261, 135154. doi: 10.1016/j.jneumeth.2015.12.004CrossRefGoogle ScholarPubMed
Landau, A. N., & Fries, P. (2012). Attention samples stimuli rhythmically. Current Biology, 22(11), 10001004. doi: 10.1016/j.cub.2012.03.054CrossRefGoogle ScholarPubMed
Lew, B. J., McDermott, T. J., Wiesman, A. I., O'Neill, J., Mills, M. S., Robertson, K. R., … Wilson, T. W. (2018). Neural dynamics of selective attention deficits in HIV-associated neurocognitive disorder. Neurology, 91(20), e1860e1869. doi: 10.1212/WNL.0000000000006504CrossRefGoogle ScholarPubMed
Lopez-Larson, M. P., Rogowska, J., & Yurgelun-Todd, D. (2015). Aberrant orbitofrontal connectivity in marijuana smoking adolescents. Developmental Cognitive Neuroscience, 16, 5462. doi: 10.1016/j.dcn.2015.08.002CrossRefGoogle ScholarPubMed
Lovell, M. E., Akhurst, J., Padgett, C., Garry, M. I., & Matthews, A. (2019). Cognitive outcomes associated with long-term, regular, recreational cannabis use in adults: A meta-analysis. Experimental and Clinical Psychopharmacology, 28(4). 10.1037/pha0000326.Google ScholarPubMed
Macaluso, E., & Patria, F. (2007). Spatial re-orienting of visual attention along the horizontal or the vertical axis. Experimental Brain Research, 180(1), 2334. doi:10.1007/s00221-006-0841-8.CrossRefGoogle ScholarPubMed
Messinis, L., Kyprianidou, A., Malefaki, S., & Papathanasopoulos, P. (2006). Neuropsychological deficits in long-term frequent cannabis users. Neurology, 66(5), 737739. doi:10.1212/01.wnl.0000201279.83203.c6.CrossRefGoogle ScholarPubMed
Morgan, N. H., Stanford, I. M., & Woodhall, G. L. (2008). Modulation of network oscillatory activity and GABAergic synaptic transmission by CB1 cannabinoid receptors in the rat medial entorhinal cortex. Neural Plasticity, 2008, 808564. doi: 10.1155/2008/808564CrossRefGoogle ScholarPubMed
Neuper, C., & Pfurtscheller, G. (2001). Event-related dynamics of cortical rhythms: Frequency-specific features and functional correlates. International Journal of Psychophysiology, 43(1), 4158. doi: 10.1016/s0167-8760(01)00178-7CrossRefGoogle ScholarPubMed
Posner, M. I. (1980). Orienting of attention. The Quarterly Journal of Experimental Psychology, 32(1), 325. doi: 10.1080/00335558008248231CrossRefGoogle ScholarPubMed
Posner, M. I. (2016). Orienting of attention: Then and now. Quarterly Journal of Experimental Psychology, 69(10), 18641875. doi: 10.1080/17470218.2014.937446CrossRefGoogle ScholarPubMed
Proskovec, A. L., Heinrichs-Graham, E., Wiesman, A. I., McDermott, T. J., & Wilson, T. W. (2018). Oscillatory dynamics in the dorsal and ventral attention networks during the reorienting of attention. Human Brain Mapping, 39(5), 21772190. doi: 10.1002/hbm.23997CrossRefGoogle ScholarPubMed
Robbe, D., Montgomery, S. M., Thome, A., Rueda-Orozco, P. E., McNaughton, B. L., & Buzsaki, G. (2006). Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nature Neuroscience, 9(12), 15261533. doi: 10.1038/nn1801CrossRefGoogle ScholarPubMed
Rossiter, H. E., Davis, E. M., Clark, E. V., Boudrias, M. H., & Ward, N. S. (2014). Beta oscillations reflect changes in motor cortex inhibition in healthy ageing. Neuroimage, 91, 360365. doi: 10.1016/j.neuroimage.2014.01.012CrossRefGoogle ScholarPubMed
Roten, A., Baker, N. L., & Gray, K. M. (2015). Cognitive performance in a placebo-controlled pharmacotherapy trial for youth with marijuana dependence. Addictive Behaviors, 45, 119123. doi:10.1016/j.addbeh.2015.01.013.CrossRefGoogle Scholar
SAMHSA (2017). Key substance use and mental health indicators in the United States: Results from the 2016 national survey on drug Use and health. Rockville, MD: Center for Behavioral Health Statistics and Quality, Substance Abuse and Mental Health Services Administration. Retrieved from https://www.samhsa.gov/data/.Google Scholar
Schreiner, A. M., & Dunn, M. E. (2012). Residual effects of cannabis use on neurocognitive performance after prolonged abstinence: A meta-analysis. Experimental and Clinical Psychopharmacology, 20(5), 420429. doi: 10.1037/a0029117CrossRefGoogle ScholarPubMed
Schweinsburg, A. D., Nagel, B. J., Schweinsburg, B. C., Park, A., Theilmann, R. J., & Tapert, S. F. (2008). Abstinent adolescent marijuana users show altered fMRI response during spatial working memory. Psychiatry Research, 163(1), 4051. doi: 10.1016/j.pscychresns.2007.04.018CrossRefGoogle ScholarPubMed
Scott, J. C., Slomiak, S. T., Jones, J. D., Rosen, A. F. G., Moore, T. M., & Gur, R. C. (2018). Association of cannabis with cognitive functioning in adolescents and young adults. JAMA Psychiatry, 75(6), 585. doi: 10.1001/jamapsychiatry.2018.0335CrossRefGoogle ScholarPubMed
Sim-Selley, L. J. (2003). Regulation of cannabinoid CB1 receptors in the central nervous system by chronic cannabinoids. Critical Reviews in Neurobiology, 15(2), 91119. doi: 10.1615/critrevneurobiol.v15.i2.10CrossRefGoogle ScholarPubMed
Skosnik, P. D., Cortes-Briones, J. A., & Hajós, M. (2016). It's all in the rhythm: The role of cannabinoids in neural oscillations and psychosis. Biological Psychiatry, 79(7), 568577. doi: 10.1016/j.biopsych.2015.12.011CrossRefGoogle ScholarPubMed
Skosnik, P. D., D'Souza, D. C., Steinmetz, A. B., Edwards, C. R., Vollmer, J. M., Hetrick, W. P., & O'Donnell, B. F. (2012). The effect of chronic cannabinoids on broadband EEG neural oscillations in humans. Neuropsychopharmacology, 37(10), 21842193. doi: 10.1038/npp.2012.65CrossRefGoogle ScholarPubMed
Spooner, R. K., Wiesman, A. I., Mills, M. S., O'Neill, J., Robertson, K. R., Fox, H. S., … Wilson, T. W. (2018). Aberrant oscillatory dynamics during somatosensory processing in HIV-infected adults. Neuroimage Clinical, 20, 8591. doi: 10.1016/j.nicl.2018.07.009CrossRefGoogle ScholarPubMed
Spooner, R. K., Wiesman, A. I., Proskovec, A. L., Heinrichs-Graham, E., & Wilson, T. W. (2019). Rhythmic spontaneous activity mediates the age-related decline in somatosensory function. Cerebral Cortex (New York, N.Y.: 1991), 29(2), 680688. doi: 10.1093/cercor/bhx349CrossRefGoogle ScholarPubMed
Spooner, R. K., Wiesman, A. I., Proskovec, A. L., Heinrichs-Graham, E., & Wilson, T. W. (2020). Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention. Human Brain Mapping, 41(2), 520529. doi: 10.1002/hbm.24819CrossRefGoogle ScholarPubMed
Taulu, S., & Simola, J. (2006). Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Physics in Medicine and Biology, 51(7), 17591768. doi: 10.1088/0031-9155/51/7/008CrossRefGoogle ScholarPubMed
Thames, A. D., Arbid, N., & Sayegh, P. (2014). Cannabis use and neurocognitive functioning in a non-clinical sample of users. Addiction Behaviors, 39(5), 994999. doi:10.1016/j.addbeh.2014.01.019.CrossRefGoogle Scholar
Thiel, C. M., Zilles, K., & Fink, G. R. (2004). Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: An event-related fMRI study. Neuroimage, 21(1), 318328. doi:10.1016/j.neuroimage.2003.08.044.CrossRefGoogle ScholarPubMed
Tzilos, G. K., Cintron, C. B., Wood, J. B., Simpson, N. S., Young, A. D., Pope, H. G. Jr., & Yurgelun-Todd, D. A. (2005). Lack of hippocampal volume change in long-term heavy cannabis users. The American Journal on Addictions, 14(1), 6472. doi:10.1080/10550490590899862CrossRefGoogle ScholarPubMed
Verdejo-García, A., Beatriz Fagundo, A., Cuenca, A., Rodriguez, J., Cuyás, E., Langohr, K., … De La Torre, R. (2013). COMT Val158met and 5-HTTLPR genetic polymorphisms moderate executive control in cannabis users. Neuropsychopharmacology, 38(8), 15981606. doi:10.1038/npp.2013.59.CrossRefGoogle ScholarPubMed
Vossel, S., Thiel, C. M., & Fink, G. R. (2006). Cue validity modulates the neural correlates of covert endogenous orienting of attention in parietal and frontal cortex. Neuroimage, 32(3), 12571264. doi: 10.1016/j.neuroimage.2006.05.019CrossRefGoogle ScholarPubMed
Vossel, S., Weidner, R., Driver, J., Friston, K. J., & Fink, G. R. (2012). Deconstructing the architecture of dorsal and ventral attention systems with dynamic causal modeling. Journal of Neuroscience, 32(31), 1063710648. doi: 10.1523/JNEUROSCI.0414-12.2012CrossRefGoogle ScholarPubMed
Weinstein, A., Livny, A., & Weizman, A. (2016). Brain imaging studies on the cognitive, pharmacological and neurobiological effects of cannabis in humans: Evidence from studies of adult users. Current Pharmaceutical Design, 22(42), 63666379. doi: 10.2174/1381612822666160822151323CrossRefGoogle ScholarPubMed
Wiesman, A. I., Groff, B. R., & Wilson, T. W. (2019). Frontoparietal networks mediate the behavioral impact of alpha inhibition in visual cortex. Cerebral Cortex (New York, N.Y.: 1991), 29(8), 35053513. doi: 10.1093/cercor/bhy220CrossRefGoogle ScholarPubMed
Wiesman, A. I., O'Neill, J., Mills, M. S., Robertson, K. R., Fox, H. S., Swindells, S., & Wilson, T. W. (2018). Aberrant occipital dynamics differentiate HIV-infected patients with and without cognitive impairment. Brain, 141(6), 16781690. doi: 10.1093/brain/awy097CrossRefGoogle ScholarPubMed
Wiesman, A. I., & Wilson, T. W. (2019). Alpha frequency entrainment reduces the effect of visual distractors. Journal of Cognitive Neuroscience, 31(9), 13921403. doi: 10.1162/jocn_a_01422CrossRefGoogle ScholarPubMed
Wilson, TW, Fleischer, A, Archer, D, Hayasaka, S, & Sawaki, L (2011). Oscillatory MEG motor activity reflects therapy-related plasticity in stroke patients. Neurorehabilitation & Neural Repair, 25(2), 188193. doi: 10.1177/1545968310378511.CrossRefGoogle ScholarPubMed
Wilson, W., Mathew, R., Turkington, T., Hawk, T., Coleman, R. E., & Provenzale, J. (2000). Brain morphological changes and early marijuana use: A magnetic resonance and positron emission tomography study. Journal of Addictive Diseases, 19(1), 122. doi: 10.1300/J069v19n01_01CrossRefGoogle ScholarPubMed
Supplementary material: Image

Springer et al. supplementary material

Springer et al. supplementary material 1

Download Springer et al. supplementary material(Image)
Image 483.8 KB
Supplementary material: Image

Springer et al. supplementary material

Springer et al. supplementary material 2

Download Springer et al. supplementary material(Image)
Image 17.6 MB
Supplementary material: File

Springer et al. supplementary material

Springer et al. supplementary material 3

Download Springer et al. supplementary material(File)
File 26.3 KB