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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. Ketamine has been used for medical purposes, most typically as an anesthetic, and recent studies support its use in the treatment of depression. However, ketamine tends to be abused by adolescents and young adults. In the current study, we examined the effects of early ketamine exposure on brain structure and function. We employed MRI to assess the effects of ketamine abuse on cerebral gray matter volume GMV and functional connectivity FC in 34 users and 19 non-users, employing covariates. Ketamine users were categorized as adolescent-onset and adult-onset based on when they were first exposed to ketamine. The results revealed lower GMV in the left precuneus in ketamine users, with a larger decrease in the adolescent-onset group. The results from a seed-based correlation analysis show that both ketamine groups had higher functional connectivity between left precuneus seed and right precuneus than the control group. These preliminary results characterize the effects of ketamine misuse on brain structure and function and highlight the influence of earlier exposure to ketamine on the development of the brain. The precuneus, a structure of central importance to cerebral functional organization, may be particularly vulnerable to the influences of early ketamine exposure. How these structural and functional brain changes may relate to the cognitive and affective deficits remains to be determined with a large cohort of participants. Substance use disorder is a chronic brain disease with peak onset occurring during adolescence. Brain imaging studies of adolescents have suggested morphological and functional changes with early exposure to substances. For example, adolescents who abuse marijuana showed decreases in whole brain volume 1 and more specifically in gray matter volume GMV in the medial orbital prefrontal cortex 2 and bilateral hippocampus 3. Adolescent substance abusers also showed impaired axonal connectivity compared to healthy controls 4. Studies demonstrated changes in cortical thickness 5 , smaller cerebellar volumes 5 , decreased hippocampal volumes 6 , 7 , and altered white matter integrity 8 in binge-drinking adolescents relative to non-drinkers. In a prospective study, heavy-drinking adolescents showed accelerated gray matter reduction in lateral frontal and temporal cortical GMV and attenuated white matter growth of the corpus callosum and pons relative to nondrinkers 9. In an fMRI study, abstinent adolescent marijuana users, as compared to non-drug using controls, showed altered brain activation during working memory 10 , 11 , 12 , verbal learning 13 , and response inhibition Adolescents with heavy alcohol use exhibited impaired visuospatial memory 15 and executive function 16 , 17 as well as deviated brain activation during visual working memory 15 , 18 and verbal encoding 19 tasks, in contrast to controls. Together, these studies provide ample evidence for structural and functional brain changes in adolescent substance abusers. Long used as an anesthetic agent for surgery, ketamine has recently been approved to treat patients with refractory depression. On the other hand, recreational use of ketamine is rapidly becoming a serious public health issue in East and Southeast Asia, including Taiwan. Since the s 20 , ketamine has been the most common abused substance in the young population. In Taiwan, a survey in shows that ketamine ranked among the top three illegal substances in school-attending adolescents, together with MDMA and marijuana The average age of first ketamine use usually falls in the junior high school period 25 , a critical period for brain development and maturation. Ketamine is much cheaper than other recreational drugs and does not appear to produce immediate, serious side effects or severe withdrawal symptoms. These characteristics may have led to its widespread use, particularly among adolescents and young adults. On the other hand, little is known about the impacts of chronic ketamine exposure on the brain. Structurally, compared with health controls, decreased GMV in bilateral frontal cortex was reported in chronic ketamine users, negatively correlated with lifetime ketamine consumption Another study revealed multiple cortical atrophies after heavy ketamine use for years, and not only in the frontal lobes This may imply broader ketamine effects on the brain. In a study with diffusion tensor imaging analysis, the ketamine users were observed to have significant reductions in fractional anisotropy over the bilateral frontal cortex and left temporoparietal cortex Edward Roberts et al. The dissociative symptoms in ketamine users were related to differences in connectivity between the caudate and the prefrontal cortex Functionally, Liao et al. In our previous functional imaging analysis of ketamine users, compared to controls, ketamine users showed higher connectivity between the caudate and dorsal anterior cingulate cortex and between the pallidum and bilateral cerebellum. In ketamine users, connectivity of the putamen was associated with both impulsivity and duration of ketamine use In a study focused on depression, ketamine users showed less sgACC connectivity to the orbitofrontal cortex OFC with increasing depression severity To our knowledge, no studies have investigated the influence of early ketamine exposure on cerebral structure and function. In this study, we examined structural and functional changes in the brains of chronic ketamine abusers, with a specific focus on distinguishing the effects of adolescent vs adult onset of ketamine use. This study was performed in accordance with the ethical guidelines and regulations suggested by the International Committee of Medical Journal Editors ICMJE such as voluntary participation, privacy protection, and assurance of confidentiality. Ketamine user KU and healthy control HC participants were recruited through posters at hospitals and online advertisements in the greater Taichung City, Taiwan. Candidates were assured at screening that their decision to participate in the study or not would not affect their right to medical care, that all personal information would be kept confidential, and that they could withdraw from the study at any time. Each participant provided a written informed consent prior to data collection. After consenting to the study, participants completed a clinical diagnostic interview with a psychiatrist, questionnaire assessments, and magnetic resonance imaging MRI All HC participants denied use of any illicit substances and showed negative urine test results None of the KU or HC participants had any major medical or neurological illnesses, history of brain concussion that resulted in loss of consciousness, or other psychiatric disorders The 17 KUs who initiated use of ketamine before age 20 were assigned to the adolescent-onset group and the 17 who started to use ketamine after age 20 were assigned to the adult-onset group. The procedures were respectively as follows: 1 the brain image was divided into segments of the GM, WM, and CSF in the native space; 2 the native space segments were affine-registered to the tissue probability maps in the Montreal Neurological Institute MNI standard space; 3 the DARTEL toolbox was used to create the group template from the affine-registered GM and WM tissue segments of all participants; 4 the GM, WM, and CSF tissue maps were modulated by the nonlinear deformation parameters obtained in the previous step; 5 the modulated segments were converted to an isotropic voxel resolution of 1. We adopted a fMRI preprocess similar to that described in a previous paper 40 and the human connectome project To address motion-related issues of the rs-fMRI, we ran not only the previous motion control analysis but also quantified framewise displacement FD to exclude participants who exhibited extreme head motion Two KUs and one HC were excluded in this latter step. A total of 34 KUs and 19 HCs were retained for the brain image analysis after the checks for head movement. The average FD values for the healthy control subjects, adult-onset ketamine users, and adolescent-onset ketamine users were 0. A mm-diameter sphere centered at each coordinate represented each seed. Pearson correlations were calculated between the BOLD time series extracted from the seed and other voxels of the whole brain using the 3dROIstats. Finally, the correlation coefficient values r were converted to z values by using the Fisher z transformation. We mainly used SPM8 for the brain image statistical analyses and examined the different effects of age, gender, and education across groups. We controlled these items by setting them as covariates for all statistical analyses. Firstly, we analyzed brain volume and functional changes between the KU and HC groups. Secondly, we further divided the KU group into two groups based on the age of first exposure to ketamine to explore the effects of different times of ketamine onset. KU adolescent onset vs. KU adult onset , covarying the confounding effects of age, years of education, and sex. F tests were performed to examine the main effects across the three groups, and post hoc t tests were performed to examine the differences between pairs of groups. For all voxel-wise statistical analyses, we addressed the problem of image-based multiple comparisons. Two-sample t tests and analysis of covariance ANCOVA were used to examine the differences between groups on participant demographic and questionnaire scores. Characteristics of the study samples are reported in Table 1. There are no significant differences in gender ratio and age in any of the groups except for a lower education level in the KU group. The average ketamine use duration of users was 4. We further divided chronic ketamine users into adolescent-onset and adult-onset groups based on their first exposure to ketamine. Within the KU group, there were no significant differences between the two onset groups in ketamine use duration, with a mean of 5. A significant difference was seen for the onset age. The adolescent-onset group started ketamine at a significantly younger age As shown in Table 3 and Fig. T-score map shows significant smaller gray matter volume in ketamine users than general adults. Bottom bar graph shows that ketamine users have decreased effect in the right insula, left inferior parietal lobule, left dorsolateral prefrontal cortex, and left medial orbitofrontal cortex. The significance level of the analyses were corrected with age, gender, and years of education as covariates. Both post hoc tests follow analysis of covariance. As for the VBM results, the left inferior parietal lobule, the left dorsolateral prefrontal cortex, and the left medial orbitofrontal cortex were defined as the seeds for the following functional connectivity analyses. The results for the other seed showed a similar tendency. T-score map showing significant functional connectivity differences between ketamine users and healthy adults. Post hoc test follow analysis of covariance. These analyses revealed significant differences in gray matter volume of the left precuneus between the KU adolescent-onset group, the KU adult-onset group, and the HC group see Fig. A one-way ANCOVA was conducted to control for the effects of age, years of education, and sex, due to there being significant differences on these covariates among the three groups. A further comparison was made of the two ketamine groups by controlling the number of years of ketamine use. F-score map showing significant differences in left precuneus for the three groups according to ketamine use onset time. The first bar graph shows the adolescent-onset group has decreased gray matter volume in left precuneus compared to the other groups bottom left. The differences remain after controlling for years of ketamine usage bottom right. We used the left precuneus as a seed for a further functional connectivity analysis. Specifically, a one-way ANCOVA was conducted to control for the effects of age, years of education, and sex due to there being significant differences on these covariates across the three groups. As shown in Table 4 and Fig. The SCA results show that both ketamine use groups had higher functional connectivity between the left precuneus seed and right precuneus than the HC group. F-score map showing significant functional connectivity differences from left precuneus to right precuneus for the three groups. The first bar graph shows that the adolescent-onset group and the adult-onset group have significantly higher functional connectivity than the control group bottom left. The group differences do not exist after controlling for years of ketamine usage bottom right. The adolescent-onset group had significantly smaller left precuneus volume than the adult-onset group. Both the adolescent-onset and adult-onset groups had increased functional connectivity between the left and right precuneus. Despite the ketamine abuse problem prevalent in some countries, few previous studies have examined changes in regional brain volume changes in chronic ketamine users. Wang et al. Liao et al. In the present study, we demonstrated decreased brain volume over the right insula, left DLPFC, left OFC, and left inferior parietal cortex in chronic ketamine users. Decreased volume of dorsal prefrontal cortex in chronic ketamine users has been reported repeatedly in brain morphology studies, a finding consistent with observations from animal studies of a neurotoxic ketamine effect in the prefrontal cortex 45 , There has been little research on resting-state functional MRI in chronic ketamine users. Interestingly, in resting fMRI and PET studies, acute ketamine infusion on health subjects also showed perturbed frontal activity 47 , 48 , Besides, a PET study provided evidence that dorsolateral prefrontal cortex D1 receptor availability was significantly up-regulated in chronic ketamine users relative to comparison subjects Imaging studies of the impact of acute ketamine infusion on frontal responses to cognitive challenges have repeatedly shown perturbations. These have been observed across a range of domains, including working memory 51 , 52 , verbal fluency 53 , and memory encoding and retrieval 53 , 54 , as well as associative learning Together, the results of these studies provide evidence that the frontal lobe may be one of the most vulnerable brain regions to both acute and chronic ketamine exposure. Although the information is not yet abundant, behavioral measurements in studies of cognitive function in chronic ketamine users show impaired verbal learning, verbal fluency, cognitive processing speed 56 and spatial working memory 57 , implying disturbance of frontal functions as well. In our study, we focused on behavioral measurements of impulsivity and depression, which typically characterize patients with addiction disorders. Studies specific to cognitive function of the prefrontal lobe, such as emotional regulation, might provide more important evidence of chronic ketamine effects. Besides, chronic ketamine abusers may not have the impaired impulse control that has been assumed. Further comprehensive evaluation of clinical profiles of chronic ketamine users would be helpful for piloting research directions. On the other hand, we demonstrated an onset-age effect of chronic ketamine use through significantly smaller left precuneus volume in the adolescent-onset group. Adolescence is a period of brain maturation characterized by greater plasticity and vulnerability. Previous studies that examined the vulnerability of the developing brain to neurotoxic consequences found that, compared to later onset groups, adolescents with early exposure to marijuana had poor performance on measures of verbal IQ 58 , attention 59 , impulse control 8 , 59 , and executive functions Moreover, studies have shown that subjects who initiated substance abuse during adolescence had more severe dependence 60 , poorer cognitive performance 59 , 61 , 62 , 63 , more profound brain morphological and functional changes 64 , 65 , more comorbidities 66 , and worse prognoses 67 , 68 than those who began their use of drugs in adults. Our results suggest that early ketamine exposure has more impact on the developing brain, a result consistent with previous findings. We could not determine the direction of causality through our cross-sectional study; whether these neural changes precipitate early-onset substance use disorder or vice-versa is a question that requires larger longitudinal studies with precise evaluation and follow-up. Ketamine is a non-competitive NMDA receptor antagonist. Previous studies have shown that the NMDA system plays an important role during this critical brain maturation period and involves several important cognitive functions. Thomases et al. Further, they carried out an animal study to demonstrate that the transient developmental disruptions during early adolescence by MK, an NMDA antagonist, can permanently alter the balance of ventral hippocampal and BLA regulation in PFC plasticity and diminish the functional capacity of prefrontal output Several mechanisms are thought to be responsible for the neural effects of ketamine in the developing brain see review First, ketamine produced greater and longer lasting blockage of NMDA receptors in immature compared to mature neurons Second, prolonged ketamine exposure produced compensatory up-regulation of NMDA receptors. This compensation may put neurons at risk of becoming more vulnerable to the excitotoxic effects of endogenous glutamate after ketamine withdrawal. Third, glutamate is crucial to certain stages of brain neuron development. Blockage of NMDA receptors in developmental stages, just for hours, could trigger widespread programmed cell death 76 , These effects are paths to greater vulnerability to ketamine-induced neurotoxicity in neurons of the developing brain. However, nearly all these data came from animal studies. Although these data provide clues about how the developing brain cells respond to ketamine influence, how the immature brain responds to prolonged or repeated ketamine exposure still needs further exploration. In this study, we demonstrated significantly smaller left precuneus volume in adolescent-onset ketamine users than in adult-onset ketamine users and healthy control subjects. Increased functional connectivity of the left precuneus was found in both the adolescent-onset and adult-onset groups. The precuneus comprises a central region of the default mode network 79 , which has the highest metabolic response during rest 80 and strong connections with adjacent and remote regions A dysfunctional default mode network has been reported in chronic cocaine users 82 , 83 , people with Internet use disorders 84 , 85 , 86 , and heroin dependent patients A recent review of addiction and precuneus function summarized evidence that the precuneus has been repeatedly implicated in exteroceptive processes, which play a critical role in the conditioned cue response in addiction In addiction studies, interoception and exteroception are frequently discussed in relation to repeated drug use behaviors. Many authors attribute sensory awareness and drug use to interoceptive processes. For example, the insular model of addiction proposed by Naqvi and Bechara 89 is focused on the addiction process transitioning from body states to conscious feelings and to decision-making processes that involve uncertain risk and reward e. Moeller et al. On the other hand, exteroception implies sensory awareness of outside stimuli; this awareness can also contribute to drug cravings such as, for example, positive and negative reinforcement of drug-seeking behaviors, cue-elicited cravings, and conditioned drug cues. Previous authors have considered the precuneus to be the core region of exteroceptive processes in addiction 88 , 91 , 92 , and it has been widely reported that it increases activation and connectivity in addicted populations In our study, we found decreased precuneus volume in adolescent-onset ketamine users and increased functional connectivity in chronic ketamine users regardless of use onset age. We may conclude that exteroceptive processes play a vital role in repetitive ketamine use behavior. In the clinical context, there are no severe symptoms of physical dependence from chronic ketamine use compared to use of other psychoactive drugs. Ketamine use is frequently influenced by peers. In some countries, ketamine abuse is almost exclusively limited to clubs and large parties Users report mood-elevation, relaxation, and near-death experiences as acute ketamine effects; these reactions may contribute to both positive and negative reinforcement of ketamine use. Our results describe the effects of chronic ketamine exposure on brain structure and function and may reflect the influence of early exposure to ketamine on the development of the brain. The precuneus, a structure of central importance to cerebral functional organization, may be a key region for producing these effects. 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Psychiatry 77 , e—e DeWitt, S. The hyper-sentient addict: an exteroception model of addiction. Drug Alcohol Abuse 41 , — Naqvi, N. The hidden island of addiction: The insula. Trends Neurosci. Moeller, S. Impaired self-awareness in human addiction: deficient attribution of personal relevance. Trends Cognit. Filbey, F. Cannabis cue-elicited craving and the reward neurocircuitry. Psychiatry 38 , 30— Grant, S. Activation of memory circuits during cue-elicited cocaine craving. De Luca, M. The role of setting for ketamine abuse: clinical and preclinical evidence. Download references. You can also search for this author in PubMed Google Scholar. All authors contributed to the discussion. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. Reprints and permissions. Hung, CC. Effects of early ketamine exposure on cerebral gray matter volume and functional connectivity. Sci Rep 10 , Download citation. Received : 09 December Accepted : 27 August Published : 23 September Anyone you share the following link with will be able to read this content:. Sorry, a shareable link is not currently available for this article. Provided by the Springer Nature SharedIt content-sharing initiative. Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily. Skip to main content Thank you for visiting nature. Download PDF. Subjects Medical research Neuroscience. Abstract Ketamine has been used for medical purposes, most typically as an anesthetic, and recent studies support its use in the treatment of depression. In vivo white matter microstructure in adolescents with early-onset psychosis: a multi-site mega-analysis Article Open access 12 December A robust and reproducible connectome fingerprint of ketamine is highly associated with the connectomic signature of antidepressants Article 23 September Introduction Substance use disorder is a chronic brain disease with peak onset occurring during adolescence. Statistical analysis We mainly used SPM8 for the brain image statistical analyses and examined the different effects of age, gender, and education across groups. Results Participants Characteristics of the study samples are reported in Table 1. Table 1 Demographic data of participants. Full size table. Table 2 Mean self-report questionnaire scores. Figure 1. Full size image. Figure 2. Figure 3. Table 4 Regional gray matter volume differences among the adolescent-onset group, adult-onset group, and control group. Figure 4. References Wilson, W. Article Google Scholar Schweinsburg, A. Article Google Scholar Ashburner, J. Article Google Scholar Marcus, D. Article Google Scholar Jenkinson, M. Article Google Scholar Smith, S. Article Google Scholar Friston, K. Article Google Scholar Fontes, M. Article Google Scholar Gruber, S. Article Google Scholar Ehrenreich, H. Article Google Scholar Kalayasiri, R. Article Google Scholar Li, Q. Article Google Scholar Filbey, F. View author publications. Ethics declarations Competing interests The authors declare no competing interests. Additional information Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. About this article. Cite this article Hung, CC. Copy to clipboard. 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Effects of early ketamine exposure on cerebral gray matter volume and functional connectivity
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