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Years of cannabis exposure as a function of spontaneous eye blink rate per minute. doi:10.1371/journal.pone.0026662.g001 

Years of cannabis exposure as a function of spontaneous eye blink rate per minute. doi:10.1371/journal.pone.0026662.g001 

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Chronic cannabis use has been shown to block long-term depression of GABA-glutamate synapses in the striatum, which is likely to reduce the extent to which endogenous cannabinoids modulate GABA- and glutamate-related neuronal activity. The current study aimed at investigating the effect of this process on striatal dopamine levels by studying the sp...

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... into the acute effect of THC on striatal DA transmission— with however inconsistent results: one study reported a THC- induced increase in striatal DA level [6] while another found no effect [7]. Things are even less clear with regard to chronic effects of long-term exposure to THC, on which no data are available. This is particularly unfortunate in view of Kuepper’s et al. [8] suggestion that repeated THC administration may create a dopaminergic imbalance in the brain by increasing striatal DA levels but lowering DA levels in prefrontal cortex. As a possible consequence of this imbalance, chronic THC exposure has been assumed to induce psychotic symptoms in users [8]. However, a problem with this assumption is that it is not based on any evidence regarding chronic effects of THC on striatal DA transmission but on only one finding regarding the acute effects [6]. Therefore, it is not clear whether THC actually induces long-term dopaminergic imbalances. To address this issue, the present study aimed at investigating the effect of long-term exposure to cannabis on striatal DA transmission. In the case of chronic effects, it is difficult to differentiate between the specific psychoactive plant components which caused the potential impairments. Consequently, we use the more generic term ‘‘cannabis’’ in the present study, even though the available data suggest that the observed effects are mainly due to the impact of THC. For one, from the two main studied psychoactive compounds of cannabis, only THC acts as a CB1 receptor agonist, while CBD functions as an antagonist. For another, CBD is suspected to reduce the psychotic effects of THC, which would suggest a role of CBD in diminishing the potential DA-impairing effects of THC [9]. Nevertheless, for the sake of precision, no reference to specific cannabinoids is made. We assessed dopaminergic functioning by means of spontaneous eye blink rates (EBR), a well-established clinical marker of striatal DA production [10–12]. Numerous observations have helped to validate EBR as a measure of striatal DA functioning. For instance, deviant levels of EBR have been reported from patients suffering from DA-related impairments: While EBR is elevated in schizophrenic patients, who exhibit increased striatal DA transmission [13], EBR is lowered in Parkinson’s patients, who have a reduced amount of nigrostriatal dopaminergic neurons [14]. In addition, EBRs vary as a function of the DRD4/7 genotype, which is associated with the modulation of DA level in the striatum [15]. Moreover, nonhuman primate research has shown that direct DA agonists and antagonists increase and decrease EBRs, respectively [16]. Exact predictions of how chronic cannabis use might affect the striatal DA level—and the associated EBR—can be derived from animal research. Hoffman et al. [17] showed that, in rats, chronic treatment with a CB1 receptor agonist results in a reduced sensitivity of CB1 receptors located at glutamatergic and GABAergic terminals. Moreover, chronic application of THC completely blocks long-term depression (LTD) of GABA-glutamate synapses in the striatum. Normally, the regulatory role of LTD is to inhibit the activity of GABA and glutamate neurons and, thus, to block their control over DA neurons, which again allows for DA transmission. Consequently, blocking LTD should reduce the extent to which endogenous cannabinoids modulate GABA and glutamate neuron activity. Moreover, the LTD-DA relationship appears to be bidirectional: striatal DA neurons are capable of synthesizing endogenous cannabinoids, which induce LTD and interact with DA as a supplementary inhibitory feedback mechanism [3,4]. However, in the case of chronic cannabis use, the decreased sensitivity of CB1 receptors implies that the likelihood of endogenous cannabinoids evoking LTD is lowered. As a result of this bidirectional process, chronic application of exogenous cannabinoids present in cannabis could be expected to lead to decreased DA transmission due to long-term, maladaptive inhibition by GABA and glutamate [17]. If so, we would expect a decrease of spontaneous EBR in chronic cannabis users as compared to non-users. EBR per minute was significantly lower in chronic cannabis users (M = 10.24; SD = 5.861) than in the non-user controls (M = 17.52; SD = 9.019), t (48) = 3.384, p , .01. The same effect was obtained in an ANOVA with group (chronic cannabis users vs. non-user controls) as independent variable and IQ and cigarette use as covariates: while the group effect was again significant, F (1, 46) = 5.477, p , .05, the covariate effects were not. To test whether the EBR in the chronic cannabis users was related to their consumption history and habits, Spearman’s Rho correlation coefficients were calculated between EBR/minute and the years of cannabis exposure, age of onset, monthly regular, monthly peak and lifetime cannabis consumption. EBR correlated negatively with years of exposure, r (25) = 2 .42, p , .05 (see Figure 1), monthly peak consumption, r (25) = 2 .43, p , .05 (see Figure 2), and lifetime consumption, r (25) = 2 .40, p , .05 (see Figure 3), while no significant correlations were found for age of onset, r (25) = 2 .04, p = n.s., and monthly regular consumption, r (25) = 2 .25, p = n.s. The results of the study show a significant reduction of spontaneous EBR in chronic cannabis users, as compared to non-user controls. This can be interpreted as an indication of a dopaminergic hypoactive state in the striatum [10–12]. Additionally, a moderate negative correlation between EBR and years of cannabis exposure suggests that the degree of impairment of DA transmission is, to a certain extent, proportional to the period of cannabis use. Conversely, the lack of a correlation between EBR and the age of onset of cannabis consumption suggests that starting to use marijuana at an earlier age does not contribute to the level of dopaminergic hypoactivity. However, such a claim should be treated with caution due to the fact that adolescent cannabis use has been linked to specific cognitive impairments, like less efficient discrimination between relevant and irrelevant stimuli [18]. In any case, it can be assumed that the striatal dopaminergic hypoactive state of chronic cannabis users is the result of blocking the supplementary inhibitory mechanism of LTD. The impairment of GABA and glutamate neuron activity combined with the down- regulation of CB1 receptors seem to be plausible explanations for the observed decreased EBR in chronic users [3,4,17]. In the case of the modest negative correlation between EBR and monthly peak cannabis use, it could be inferred that a more pronounced binge use of marijuana has an additional detrimental impact on the level of DA in the striatum. However, DA impairment was found not to be related to the regular amount of cannabis consumed per month. A possible explanation for this effect comes from the research by Bolla et al. [19], who identified organic drug exposure intensity, instead of duration, as a key factor in developing drug-related neurocognitive deterioration. Therefore, it seems plausible to assume that binge use of cannabis is a better predictor of DA impairment than regular consumption. Additionally, the moderate negative correlation between EBR and lifetime cannabis consumption suggests that the degree of impairment of striatal dopaminergic functioning is related to the total amount of cannabis consumed during lifetime. Possibly, use of higher doses of cannabis, both in the short- and long-term, has a more detrimental enduring effect on GABA and glutamate inhibition of DA in striatum, as compared to the impact of using smaller doses for a longer period of time. As for limitations of the present study, one is the lack of additional verification of participants’ compliance with the no- consumption instructions. Subjects’ urinary or plasma levels of THC metabolites (THC-COOH) were not examined to confirm cannabis use status. Another limitation is the correlative nature of the study, which does not preclude causal contributions from possible self-selection factors, such as a predisposition for low striatal DA production that seduces people to use cannabis. It may also be suspected that significantly more nicotine smokers in the chronic cannabis condition might have contributed to the difference in the observed EBR between groups. However, not only did the critical effect survive the input of nicotine use as covariate but research also indicates that the long-term effect of nicotine on DA is facilitatory rather than inhibitory [20]. This suggests that, in anything, the observed reduction in EBR provides a rather conservative estimate of the association between cannabis use and striatal DA levels. Concluding, the results of the present study point to less efficient striatal dopaminergic functioning in chronic cannabis users. This finding seems crucial in understanding the suspected psychotic effects of long-term cannabis use and throws some doubts on the claim that cannabis-induced psychosis results from the combina- tion of increased striatal and reduced prefrontal DA levels [8]. Additionally, the fact that cannabis has an indirect effect on DA implies caution in predictions of DA-related disorders due to chronic cannabis use. As a result of dopaminergic neurons not being impaired by cannabinoids, long-term consequences of cannabis exposure may be less severe than in the case of drugs directly damaging dopaminergic cells, like cocaine (for a discussion, see [5]). More research is required in order to identify the neurophysiological and cognitive effects of continuous marijuana use, which are likely to be more subtle than in the case of other recreational drugs. Fifty-three healthy adults served as participants, 28 chronic cannabis users and 25 non-user controls. Participants received either course credit or financial reward. The sample was obtained from the city of Leiden using ...

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... Indeed, reduction in sEBR following dopamine antagonist administration as well as an increase after dopamine agonist administration was observed [18][19][20][21]. sEBR was also linked to changes in dopamine regulation in several neurological and psychiatric disorders [22][23][24], including substance use disorders [25,26]. Previous studies have also shown a relationship between sEBR and cognitive functions such as attention and cognitive flexibility [27]. ...
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