Automated Detection of Cognitive Performance and Resilience Changes in Former Professional American Football Players Following the Administration of a Hemp Extract

  • Francesco Amico
  • Annalisa Pascarella
  • Slav Danev
  • Cheng Ruan Texas Center for Lifestyle Medicine
Keywords: sports concussion, American football, EEG, ERP, CBD, CBG


Introduction. In high-contact sport athletes, repetitive head trauma might be linked to permanent brain damage. In particular, findings in professional American football players indicate that brain injury is often associated with long-term cognitive slowing. In this context, hemp extracts might have beneficial effects. Methods. Forty-two former professional American football players were recruited (age = 49.6 ± 9.8 years). Before or immediately after the oral administration of a THC-free hemp extract, the following measures were acquired: 1) the median theta/beta ratio and posterior peak alpha frequency (PAF) during resting state; 2) P200 and P300b latencies as well as reaction times (RT) during performance of a Go/NoGo task. Results. After treatment, a smaller median theta/beta ratio (p < .01) was detected. An onset latency reduction was also found for the P200 (p < .01) and P300b (p < .05) measures, which was accompanied by smaller RT variances (p < .05). Finally, a positive correlation between RT measures and P300b latencies was found only after treatment. Conclusion. The administration of THC-free hemp extracts in former professional high-impact athletes might have beneficial effects on both cognitive performance and emotion regulation. Also, recent technological advances in EEG detection and analysis could play an important role in the management of patients with sport-related brain injuries.


Al-Fahoum, A. S., & Al-Fraihat, A. A. (2014). Methods of EEG signal features extraction using linear analysis in frequency and time-frequency domains. International Scholarly Research Notices, 2014, 730218.

Alosco, M. L., Tripodis, Y., Fritts, N. G., Heslegrave, A., Baugh, C. M., Conneely, S., Mariani, M., Martin, B. M., Frank, S., Mez, J., Stein, T. D., Cantu, R. C., McKee, A. C., Shaw, L. M., Trojanowski, J. Q., Blennow, K., Zetterberg, H., & Stern, R. A. (2018). Cerebrospinal fluid tau, Aβ, and sTREM2 in former National Football League players: Modeling the relationship between repetitive head impacts, microglial activation, and neurodegeneration. Alzheimer’s & Dementia, 14(9), 1159–1170.

Alosco, M. L., Tripodis, Y., Rowland, B., Chua, A. S., Liao, H., Martin, B., Jarnagin, J., Chaisson, C. E., Pasternak, O., Karmacharya, S., Koerte, I. K., Cantu, R. C., Kowall, N. W., McKee, A. C., Shenton, M. E., Greenwald, R., McClean, M., Stern, R. A., & Lin, A. (2020). A magnetic resonance spectroscopy investigation in symptomatic former NFL players. Brain Imaging and Behavior, 14(5), 1419–1429.

Alvarez, F. J., Lafuente, H., Rey-Santano, M. C., Mielgo, V. E., Gastiasoro, E., Rueda, M., Pertwee, R. G., Castillo, A. I., Romero, J., & Martinez-Orgado, J. (2008). Neuroprotective effects of the nonpsychoactive cannabinoid cannabidiol in hypoxic-ischemic newborn piglets. Pediatric Research, 64(6), 653–658.

Angelakis, E., Lubar, J. F., & Stathopoulou, S. (2004). Electroencephalographic peak alpha frequency correlates of cognitive traits. Neuroscience Letters, 371(1), 60–63.

Angelakis, E., Lubar, J. F., Stathopoulou, S., & Kounios, J. (2004). Peak alpha frequency: An electroencephalographic measure of cognitive preparedness. Clinical Neurophysiology, 115(4), 887–897.

Angelakis, E., Stathopoulou, S., Frymiare, J. L., Green, D. L., Lubar, J. F., & Kounios, J. (2007). EEG neurofeedback: A brief overview and an example of peak alpha frequency training for cognitive enhancement in the elderly. The Clinical Neuropsychologist, 21(1), 110–129.

Arnsten, A. F. T. (2010). The use of α-2A adrenergic agonists for the treatment of attention-deficit/hyperactivity disorder. Expert Review of Neurotherapeutics, 10(10), 1595–1605.

Aurlien, H., Gjerde, I. O., Aarseth, J. H., Eldøen, G., Karlsen, B., Skeidsvoll, H., & Gilhus, N. E. (2004). EEG background activity described by a large computerized database. Clinical Neurophysiology, 115(3), 665–673.

Baillargeon, A., Lassonde, M., Leclerc, S., & Ellemberg, D. (2012). Neuropsychological and neurophysiological assessment of sport concussion in children, adolescents and adults. Brain Injury, 26(3), 211–220.

Baron, E. P. (2018). Medicinal properties of cannabinoids, terpenes, and flavonoids in cannabis, and benefits in migraine, headache, and pain: An update on current evidence and cannabis science. Headache, 58(7), 1139–1186.

Bazanova, O. M., & Vernon, D. (2014). Interpreting EEG alpha activity. Neurosci ence & Biobehavioral Reviews, 44, 94–110.

Benito, C., Kim, W.-K., Chavarría, I., Hillard, C. J., Mackie, K., Tolón, R. M., Williams, K., & Romero, J. (2005). A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis. The Journal of Neuroscience, 25(10), 2530–2536.

Borck, C. (2005). Writing brains: Tracing the psyche with the graphical method. History of Psychology, 8(1), 79–94.

Borgan, F., Beck, K., Butler, E., McCutcheon, R., Veronese, M., Vernon, A., & Howes, O. D. (2019). The effects of cannabinoid 1 receptor compounds on memory: A meta-analysis and systematic review across species. Psychopharmacology, 236(11), 3257–3270.

Bowles, E. J. (2003). The Chemistry of Aromatherapeutic Oils, 3rd Edition. Crows Nest, NSW, Australia: Allen & Unwin.

Campos, A. C., Fogaça, M. V., Sonego, A. B., & Guimarães, F. S. (2016). Cannabidiol, neuroprotection and neuropsychiatric disorders. Pharmacological Research, 112, 119–127.

Cascio, M. G., Gauson, L. A., Stevenson, L. A., Ross, R. A., & Pertwee, R. G. (2010). Evidence that the plant cannabinoid cannabigerol is a highly potent α2-adrenoceptor agonist and moderately potent 5HT1A receptor antagonist. British Journal of Pharmacology, 159(1), 129–141.

Cassano, T., Calcagnini, S., Pace, L., De Marco, F., Romano, A., & Gaetani, S. (2017). Cannabinoid receptor 2 signaling in neurodegenerative disorders: From pathogenesis to a promising therapeutic target. Frontiers in Neuroscience, 11, 30.

Changa, A. R., Vietrogoski, R. A., & Carmel, P. W. (2018). Dr Harrison Martland and the history of punch drunk syndrome. Brain, 141(1), 318–321.

Chiang, A. K. I., Rennie, C. J., Robinson, P. A., van Albada, S. J., & Kerr, C. C. (2011). Age trends and sex differences of alpha rhythms including split alpha peaks. Clinical Neurophysiology, 122(8), 1505–1517.

Clark, M., & Guskiewicz, K. (2016). Sport-related traumatic brain injury. In D. Laskowitz & G. Grant (Eds.), Translational research in traumatic brain injury. Boca Raton, FL: CRC Press/Taylor and Francis Group.

Clarke, A. R., Barry, R. J., McCarthy, R., & Selikowitz, M. (2001). EEG-defined subtypes of children with attention-deficit/hyperactivity disorder. Clinical Neurophysiology, 112(11), 2098–2105.

Clarke, A. R., Barry, R. J., McCarthy, R., Selikowitz, M., Brown, C. R., & Croft, R. J. (2003). Effects of stimulant medications on the EEG of children with attention-deficit/hyperactivity disorder predominantly inattentive type. International Journal of Psychophysiology, 47(2), 129–137.

Collura, T. F. (1993). History and evolution of electroencephalographic instruments and techniques. Journal of Clinical Neurophysiology, 10(4), 476–504.

De Petrocellis, L., Ligresti, A., Moriello, A. S., Allarà, M., Bisogno, T., Petrosino, S., Stott, C. G., & Di Marzo, V. (2011). Effects of cannabinoids and cannabinoid-enriched cannabis extracts on TRP channels and endocannabinoid metabolic enzymes. British Journal of Pharmacology, 163(7), 1479–1494.

De Petrocellis, L., Orlando, P., Moriello, A. S., Aviello, G., Stott, C., Izzo, A. A., & Di Marzo, V. (2012). Cannabinoid actions at TRPV channels: Effects on TRPV3 and TRPV4 and their potential relevance to gastrointestinal inflammation. Acta Physiologica, 204(2), 255–266.

Dobrakowski, P., & Lebecka, G. (2020). Individualized neurofeedback training may help achieve long-term improvement of working memory in children with ADHD. Clinical EEG and Neuroscience, 51(2), 94–101.

Duncan-Johnson, C. C., & Donchin, E. (1980). The relation of P300 latency to reaction time as a function of expectancy. Progress in Brain Research, 54, 717–722.

Duncan-Johnson, C. C., & Donchin, E. (1982). The P300 component of the event-related brain potential as an index of information processing. Biological Psychology, 14(1–2), 1–52.

Echeverry, C., Prunell, G., Narbondo, C., de Medina, V. S., Nadal, X., Reyes-Parada, M., & Scorza, C. (2021). A comparative in vitro study of the neuroprotective effect induced by cannabidiol, cannabigerol, and their respective acid forms: Relevance of the 5-HT1A receptors. Neurotoxicity Research, 39(2), 335–348.

Ernsberger, P., Giuliano, R., Willette, R. N., & Reis, D. J. (1990). Role of imidazole receptors in the vasodepressor response to clonidine analogs in the rostral ventrolateral medulla. Journal of Pharmacology and Experimental Therapeutics, 253(1), 408–418.

Felmingham, K. L., Baguley, I. J., & Green, A. M. (2004). Effects of diffuse axonal injury on speed of information processing following severe traumatic brain injury. Neuropsychology, 18(3), 564–571.

Fernández-Ruiz, J., Sagredo, O., Pazos, M. R., García, C., Pertwee, R., Mechoulam, R., & Martínez-Orgado, J. (2013). Cannabidiol for neurodegenerative disorders: Important new clinical applications for this phytocannabinoid? British Journal of Clinical Pharmacology, 75(2), 323–333.

Ferraro, F. R. (1996). Cognitive slowing in closed-head injury. Brain and Cognition, 32(3), 429–440.

Garavan, H., Ross, T. J., Murphy, K., Roche, R. A. P., & Stein, E. A. (2002). Dissociable executive functions in the dynamic control of behavior: Inhibition, error detection, and correction. NeuroImage, 17(4), 1820–1829.

Gertler, R., Brown, H. C., Mitchell, D. H., & Silvius, E. N. (2001). Dexmedetomidine: A novel sedative-analgesic agent. Baylor University Medical Center Proceedings, 14(1), 13–21.

Ghajar, J., & Ivry, R. B. (2008). The predictive brain state: Timing deficiency in traumatic brain injury? Neurorehabilitation and Neural Repair, 22(3), 217–227.

Gomes, J., & Damborská, A. (2017). Event-Related potentials as biomarkers of mild traumatic brain injury. Activitas Nervosa Superior, 59, 87–90.

Gómez del Pulgar, T., de Ceballos, M. L., Guzmán, M., & Velasco, G. (2002). Cannabinoids protect astrocytes from ceramide-induced apoptosis through the phosphatidylinositol 3-kinase/protein kinase B pathway. Journal of Biological Chemistry, 277(39), 36527–36533.

Gorus, E., De Raedt, R., Lambert, M., Lemper, J. C., & Mets, T. (2008). Reaction times and performance variability in normal aging, mild cognitive impairment, and Alzheimer's disease. Journal of Geriatric Psychiatry and Neurology, 21(3), 204–218.

Gosselin, N., Bottari, C., Chen, J.-K., Huntgeburth, S. C., De Beaumont, L., Petrides, M., Cheung, B., & Ptito, A. (2012). Evaluating the cognitive consequences of mild traumatic brain injury and concussion by using electrophysiology. Neurosurgical Focus, 33(6), E7: 1–7.

Grandy, T. H., Werkle-Bergner, M., Chicherio, C., Schmiedek, F., Lövdén, M., & Lindenberger, U. (2013). Peak individual alpha frequency qualifies as a stable neurophysiological trait marker in healthy younger and older adults. Psychophysiology, 50(6), 570–582.

Gugliandolo, A., Silvestro, S., Chiricosta, L., Pollastro, F., Bramanti, P., & Mazzon, E. (2020). The transcriptomic analysis of NSC-34 motor neuron-like cells reveals that cannabigerol influences synaptic pathways: A comparative study with cannabidiol. Life, 10(10), 227.

Gulluni, N., Re, T., Loiacono, I., Lanzo, G., Gori, L., Macchi, C., Epifani, F., Bragazzi, N., & Firenzuoli, F. (2018). Cannabis essential oil: A preliminary study for the evaluation of the brain effects. Evidence-Based Complementary Alternative Medicine, 2018, 1709182.

Guskiewicz, K. M., Marshall, S. W., Bailes, J., McCrea, M., Cantu, R. C., Randolph, C., & Jordan, B. D. (2005). Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery, 57(4), 719–726.

Hampton, A., & Weber-Fox, C. (2008). Non-linguistic auditory processing in stuttering: Evidence from behavior and event-related brain potentials. Journal of Fluency Disorders, 33(4), 253–273.

Hart, J., Jr., Kraut, M. A., Womack, K. B., Strain, J., Didehbani, N., Bartz, E., Conover, H., Mansinghani, S., Lu, H., & Cullum, C. M. (2013). Neuroimaging of cognitive dysfunction and depression in aging retired National Football League players: A cross-sectional study. JAMA Neurology, 70(3), 326–335.

Hayakawa, K., Mishima, K., & Fujiwara, M. (2010). Therapeutic potential of non-psychotropic cannabidiol in ischemic stroke. Pharmaceuticals, 3(7), 2197–2212.

Heuberger, E., Hongratanaworakit, T., Böhm, C., Weber, R., & Buchbauer, G. (2001). Effects of chiral fragrances on human autonomic nervous system parameters and self-evaluation. Chemical Senses, 26(3), 281–292.

Hunter, J. C., Fontana, D. J., Hedley, L. R., Jasper, J. R., Lewis, R., Link, R. E., Secchi, R., Sutton, J., & Eglen, R. M. (1997). Assessment of the role of α2-adrenoceptor subtypes in the antinociceptive, sedative and hypothermic action of dexmedetomidine in transgenic mice. British Journal of Pharmacology, 122(7), 1339–1344.

Husnu Can Baser, K., & Buchbauer, G. (2015). Biological activities of essential oils: An update (2nd ed.). Boca Raton, FL: CRC Press.

Immke, D. C., & Gavva, N. R. (2006). The TRPV1 receptor and nociception. Seminars in Cell & Developmental Biology, 17(5), 582–591.

Iriarte, J., Urrestarazu, E., Valencia, M., Alegre, M., Malanda, A., Viteri, C., & Artieda, J. (2003). Independent component analysis as a tool to eliminate artifacts in EEG: A quantitative study. Journal of Clinical Neurophysiology, 20(4), 249–257.

Jeong, S.-I., Lim, J.-P., & Jeon, H. (2007). Chemical composition and antibacterial activities of the essential oil from Abies koreana. Phytotherapy Research, 21(12), 1246–1250.

Jiang, X., Bian, G.-B., & Tian, Z. (2019). Removal of artifacts from EEG signals: A review. Sensors, 19(5), 987.

Jorge, R. E., Starkstein, S. E., Arndt, S., Moser, D., Crespo-Facorro, B., & Robinson, R. G. (2005). Alcohol misuse and mood disorders following traumatic brain injury. Archives of General Psychiatry, 62(7), 742–749.

Key, A. P. F., Dove, G. O., & Maguire, M. J. (2005). Linking brainwaves to the brain: An ERP primer. Developmental Neuropsychology, 27(2), 183–215.

Kim, E., Lauterbach, E. C., Reeve, A., Arciniegas, D. B., Coburn, K. L., Mendez, M. F., Rummans, T. A., & Coffey, E. C. (2007). Neuropsychiatric complications of traumatic brain injury: A critical review of the literature (a report by the ANPA Committee on Research). The Journal of Neuropsychiatry and Clinical Neurosciences, 19(2), 106–127.

Kim, K., Bu, Y., Jeong, S., Lim, J., Kwon, Y., Cha, D. S., Kim, J., Jeon, S., Eun, J., & Jeon, H. (2006). Memory-enhancing effect of a supercritical carbon dioxide fluid extract of the needles of Abies koreana on scopolamine-induced amnesia in mice. Bioscience, Biotechnology, and Biochemistry, 70(8), 1821–1826.

Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis. Brain Research Reviews, 29(2–3), 169–195.

Kothari, R., Bokariya, P., Singh, S., & Singh, R. (2016). A comprehensive review on methodologies employed for visual evoked potentials. Scientifica, 2016, 9852194.

Kozela, E., Juknat, A., & Vogel, Z. (2017). Modulation of astrocyte activity by cannabidiol, a nonpsychoactive cannabinoid. International Journal of Molecular Sciences, 18(8), 1669.

Kutas, M., McCarthy, G., & Donchin, E. (1977). Augmenting mental chronometry: The P300 as a measure of stimulus evaluation time. Science, 197(4305), 792–795.

Levine, B., Fujiwara, E., O'Connor, C., Richard, N., Kovacevic, N., Mandic, M., Restagno, A., Easdon, C., Robertson, I. H., Graham, S. J., Cheung, G., Gao, F., Schwartz, M. L., & Black, S. E. (2006). In vivo characterization of traumatic brain injury neuropathology with structural and functional neuroimaging. Journal of Neurotrauma, 23(10), 1396–1411.

Ling, H., Hardy, J., & Zetterberg, H. (2015). Neurological consequences of traumatic brain injuries in sports. Molecular and Cell Neuroscience, 66(Pt. B), 114–122.

Lorenzetti, B. B., Souza, G. E., Sarti, S. J., Santos Filho, D., & Ferreira, S. H. (1991). Myrcene mimics the peripheral analgesic activity of lemongrass tea. Journal of Ethnopharmacology, 34(1), 43–48.

Lu, H.-C., & Mackie, K. (2016). An introduction to the endogenous cannabinoid system. Biological Psychiatry, 79(7), 516–525.

Manley, G., Gardner, A. J., Schneider, K. J., Guskiewicz, K. M., Bailes, J., Cantu, R. C., Castellani, R. J., Turner, M., Jordan, B. D., Randolph, C., Dvořák, J., Hayden, K. A., Tator, C. H., McCrory, P., & Iverson, G. L. (2017). A systematic review of potential long-term effects of sport-related concussion. British Journal of Sports Medicine, 51(12), 969–977.

Markiewcz, R. (2017). The use of EEG biofeedback/neurofeedback in psychiatric rehabilitation. Psychiatria Polska, 51(6), 1095–1106.

Marlats, F., Djabelkhir-Jemmi, L., Azabou, E., Boubaya, M., Pouwels, S., & Rigaud, A.-S. (2019). Comparison of effects between SMR/delta-ratio and beta1/theta-ratio neurofeedback training for older adults with Mild Cognitive Impairment: A protocol for a randomized controlled trial. Trials, 20(1), 88.

Mathias, J. L., Beall, J. A., & Bigler, E. D. (2004). Neuropsychological and information processing deficits following mild traumatic brain injury. Journal of the International Neuropsychological Society, 10(2), 286–297.

Mathias, J. L., & Wheaton, P. (2007). Changes in attention and information-processing speed following severe traumatic brain injury: A meta-analytic review. Neuropsychology, 21(2), 212–223.

McKee, A. C., Abdolmohammadi, B., & Stein, T. D. (2018). The neuropathology of chronic traumatic encephalopathy. Handbook of Clinical Neurology, 158, 297–307.

McWilliams, J., & Schmitter-Edgecombe, M. (2008). Semantic memory organization during the early stage of recovery from traumatic brain injury. Brain Injury, 22(3), 243–253.

Miranda, P., Cox, C. D., Alexander, M., Danev, S., & Lakey, J. R. T. (2019). Overview of current diagnostic, prognostic, and therapeutic use of EEG and EEG-based markers of cognition, mental, and brain health. Integrative Molecular Medicine, 6, 1–9.

Molina-Holgado, E., Vela, J. M., Arévalo-Martin, A., Almazán, G., Molina-Holgado, F., Borrell, J., & Guaza, C. (2002). Cannabinoids promote oligodendrocyte progenitor survival: Involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. The Journal of Neuroscience, 22(22), 9742–9753.

Moore, R. D., Lepine, J., & Ellemberg, D. (2017). The independent influence of concussive and sub-concussive impacts on soccer players' neurophysiological and neuropsychological function. International Journal of Psychophysiology, 112, 22–30.

Muller, C., Morales, P., & Reggio, P. H. (2018). Cannabinoid ligands targeting TRP channels. Frontiers in Molecular Neuroscience, 11, 487.

Navarrete, M., Díez, A., & Araque, A. (2014). Astrocytes in endocannabinoid signalling. Philosophical Transactions of the Royal Society B Biological Sciences, 369(1654), 20130599.

Navarro, G., Varani, K., Lillo, A., Vincenzi, F., Rivas-Santisteban, R., Raïch, I., Reyes-Resina, I., Ferreiro-Vera, C., Borea, P. A., Sánchez de Medina, V., Nadal, X., & Franco, R. (2020). Pharmacological data of cannabidiol- and cannabigerol-type phytocannabinoids acting on cannabinoid CB1, CB2 and CB1/CB2 heteromer receptors. Pharmacological Research, 159, 104940.

Navarro, G., Varani, K., Reyes-Resina, I., Sánchez de Medina, V., Rivas-Santisteban, R., Sánchez-Carnerero Callado, C., Vincenzi, F., Casano, S., Ferreiro-Vera, C., Canela, E. I., Borea, P. A., Nadal, X., & Franco, R. (2018). Cannabigerol action at cannabinoid CB1 and CB2 receptors and at CB1-CB2 heteroreceptor complexes. Frontiers in Pharmacology, 9, 632.

Panikashvili, D., Simeonidou, C., Ben-Shabat, S., Hanuš, L., Breuer, A., Mechoulam, R., & Shohami, E. (2001). An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature, 413(6855), 527–531.

Papathanasiou, E. S., Cronin, T., Seemungal, B., & Sandhu, J. (2018). Electrophysiological testing in concussion: A guide to clinical applications. Journal of Concussion, 2.

Pelegrín-Valero, C. A., Gómez-Hernández, R., Muñoz-Céspedes, J. M., Fernández-Guinea, S. D., & Tirapu-Ustarroz, J. (2001). Consideraciones nosológicas del cambio de personalidad postraumático [Nosologic aspects of personality change due to head trauma]. Revista de Neurología, 32(7), 681–687.

Pertwee, R. G. (2008). The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: Δ9 tetrahydrocannabinol, cannabidiol and Δ9 tetrahydrocannabivarin. British Journal of Pharmacology, 153(2), 199–215.

Polich, J. (2007). Updating P300: An integrative theory of P3a and P3b. Clinical Neurophysiology, 118(10), 2128–2148.

Pollastro, F., Taglialatela-Scafati, O., Allarà, M., Muñoz, E., Di Marzo, V., De Petrocellis, L., & Appendino, G. (2011). Bioactive prenylogous cannabinoid from fiber hemp (cannabis sativa). Journal of Natural Products, 74(9), 2019–2022.

Posthuma, D., Neale, M. C., Boomsma, D. I., & de Geus, E. J. (2001). Are smarter brains running faster? Heritability of alpha peak frequency, IQ, and their interrelation. Behavior Genetics, 31(6), 567–579.

Randolph, C., Karantzoulis, S., & Guskiewicz, K. (2013). Prevalence and characterization of mild cognitive impairment in retired National Football League players. Journal of International Neuropsychological Society, 19(8), 873–880.

Ridet, J. L., Privat, A., Malhotra, S. K., & Gage, F. H. (1997). Reactive astrocytes: Cellular and molecular cues to biological function. Trends in Neurosciences, 20(12), 570–577.

Ríos, M., Periañez, J. A., & Muñoz-Céspedes, J. M. (2004). Attentional control and slowness of information processing after severe traumatic brain injury. Brain Injury, 18(3), 257–272.

Rock, E. M., Bolognini, D., Limebeer, C. L., Cascio, M. G., Anavi-Goffer, S., Fletcher, P. J., Mechoulam, R., Pertwee, R. G., & Parker, L. A. (2012). Cannabidiol, a non-psychotropic component of cannabis, attenuates vomiting and nausea-like behaviour via indirect agonism of 5-HT1A somatodendritic autoreceptors in the dorsal raphe nucleus. British Journal of Pharmacology, 165(8), 2620–2634.

Rock, E. M., Goodwin, J. M., Limebeer, C. L., Breuer, A., Pertwee, R. G., Mechoulam, R., & Parker, L. A. (2011). Interaction between non-psychotropic cannabinoids in marihuana: Effect of cannabigerol (CBG) on the anti-nausea or anti-emetic effects of cannabidiol (CBD) in rats and shrews. Psychopharmacology, 215(3), 505–512.

Rosenthaler, S., Pöhn, B., Kolmanz, C., Huu, C. N., Krewenka, C., Huber, A., Kranner, B., Rausch, W.-D., & Moldzio, R. (2014). Differences in receptor binding affinity of several phytocannabinoids do not explain their effects on neural cell cultures. Neurotoxicology and Teratology, 46, 49–56.

Roser, P., Juckel, G., Rentzsch, J., Nadulski, T., Gallinat, J., & Stadelmann, A. M. (2008). Effects of acute oral Δ9 tetrahydrocannabinol and standardized cannabis extract on the auditory P300 event-related potential in healthy volunteers. European Neuropsychopharmacology, 18(8), 569–577.

Rule, R. R., Shimamura, A. P., & Knight, R. T. (2002). Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cognitive, Affective, & Behavioral Neuroscience, 2(3), 264–270.

Russo, E. B. (2011). Taming THC: Potential cannabis synergy and phytocannabinoid-terpenoid entourage effects. British Journal of Pharmacology, 163(7), 1344–1364.

Russo, E. B., Burnett, A., Hall, B., & Parker, K. K. (2005). Agonistic properties of cannabidiol at 5-HT1a receptors. Neurochemical Research, 30(8), 1037–1043.

Sachdev, P., Smith, J. S., & Cathcart, S. (2001). Schizophrenia-like psychosis following traumatic brain injury: A chart-based descriptive and case-control study. Psychological Medicine, 31(2), 231–239.

Sari, B. A., Koster, E. H. W., Pourtois, G., & Derakshan, N. (2016). Training working memory to improve attentional control in anxiety: A proof-of-principle study using behavioral and electrophysiological measures. Biological Psychology, 121(Pt. B), 203–212.

Schurman, L. D., & Lichtman, A. H. (2017). Endocannabinoids: A promising impact for traumatic brain injury. Frontiers in Pharmacology, 8, 69.

Schutter, D. J. L. G., & Van Honk, J. (2005). Electrophysiological ratio markers for the balance between reward and punishment. Cognitive Brain Research, 24(3), 685–690.

Seo, M., Sowndhararajan, K., & Kim, S. (2016). Influence of binasal and uninasal inhalations of essential oil of Abies koreana twigs on electroencephalographic activity of human. Behavioural Neurology, 2016, 9250935.

Shah, S. A., Goldin, Y., Conte, M. M., Goldfine, A. M., Mohamadpour, M., Fidali, B. C., Cicerone, K., & Schiff, N. D. (2017). Executive attention deficits after traumatic brain injury reflect impaired recruitment of resources. NeuroImage: Clinical, 14, 233–241.

Shapiro, S. S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3–4), 591–611.

Shohami, E., Cohen-Yeshurun, A., Magid, L., Algali, M., & Mechoulam, R. (2011). Endocannabinoids and traumatic brain injury. British Journal of Pharmacology, 163(7), 1402–1410.

Smit, C. M., Wright, M. J., Hansell, N. K., Geffen, G. M., & Martin, N. G. (2006). Genetic variation of individual alpha frequency (IAF) and alpha power in a large adolescent twin sample. International Journal of Psychophysiology, 61(2), 235–243.

Stella, N. (2010). Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia, 58(9), 1017–1030.

Strain, J., Didehbani, N., Cullum, C. M., Mansinghani, S., Conover, H., Kraut, M. A., Hart, J., & Womack, K. B. (2013). Depressive symptoms and white matter dysfunction in retired NFL players with concussion history. Neurology, 81(1), 25–32.

Szabo, B., & Schlicker, E. (2005). Effects of cannabinoids on neurotransmission. In R. G. Pertwee (Ed.), Cannabinoids. Handbook of experimental pharmacology (vol. 168, pp. 327–365). Springer Berlin, Heidelberg.

Tateno, A., Jorge, R. E., & Robinson, R. G. (2003). Clinical correlates of aggressive behavior after traumatic brain injury. The Journal of Neuropsychiatry and Clinical Neurosciences, 15(2), 155–160.

Tateno, A., Jorge, R. E., & Robinson, R. G. (2004). Pathological laughing and crying following traumatic brain injury. The Journal of Neuropsychiatry and Clinical Neurosciences, 16(4), 426–434.

Thériault, M., De Beaumont, L., Gosselin, N., Filipinni, M., & Lassonde, M. (2009). Electrophysiological abnormalities in well functioning multiple concussed athletes. Brain Injury, 23(11), 899–906.

van Reekum, R., Cohen, T., & Wong, J. (2000). Can traumatic brain injury cause psychiatric disorders? The Journal of Neuropsychiatry and Clinical Neurosciences, 12(3), 316–327.

van Tricht, M. J., Harmsen, E. C., Koelman, J. H. T. M., Bour, L. J., van Amelsvoort, T. A., Linszen, D. H., de Haan, L. & Nieman, D. H. (2013). Effects of cannabis use on event related potentials in subjects at ultra high risk for psychosis and healthy controls. International Journal of Psychophysiology, 88(2), 149–156.

Vázquez, C., Tolón, R. M., Pazos, M. R., Moreno, M., Koester, E. C., Cravatt, B. F., Hillard, C. J., & Romero, J. (2015). Endocannabinoids regulate the activity of astrocytic hemichannels and the microglial response against an injury: In vivo studies. Neurobiology of Disease, 79, 41–50.

Walter, L., & Stella, N. (2004). Cannabinoids and neuroinflammation. British Journal of Pharmacology, 141(5), 775–785.

Whitley, E., & Ball, J. (2002). Statistics review 6: Nonparametric methods. Critical Care, 6(6), 509–513.

Yao, Z.-F., & Hsieh, S. (2019). Neurocognitive mechanism of human resilience: A conceptual framework and empirical review. International Journal of Environmental Research and Public Health, 16(24), 5123.

Zeilig, G., Drubach, D. A., Katz-Zeilig, M., & Karatinos, J. (1996). Pathological laughter and crying in patients with closed traumatic brain injury. Brain Injury, 10(8), 591–597.

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