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Increased functional connectivity in the resting-state basal ganglia network after acute heroin substitution.

ABSTRACT: Reinforcement signals in the striatum are known to be crucial for mediating the subjective rewarding effects of acute drug intake. It is proposed that these effects may be more involved in early phases of drug addiction, whereas negative reinforcement effects may occur more in later stages of the illness. This study used resting-state functional magnetic resonance imaging to explore whether acute heroin substitution also induced positive reinforcement effects in striatal brain regions of protracted heroin-maintained patients. Using independent component analysis and a dual regression approach, we compared resting-state functional connectivity (rsFC) strengths within the basal ganglia/limbic network across a group of heroin-dependent patients receiving both an acute infusion of heroin and placebo and 20 healthy subjects who received placebo only. Subsequent correlation analyses were performed to test whether the rsFC strength under heroin exposure correlated with the subjective rewarding effect and with plasma concentrations of heroin and its main metabolites morphine. Relative to the placebo treatment in patients, heroin significantly increased rsFC of the left putamen within the basal ganglia/limbic network, the extent of which correlated positively with patients' feelings of rush and with the plasma level of morphine. Furthermore, healthy controls revealed increased rsFC of the posterior cingulate cortex/precuneus in this network relative to the placebo treatment in patients. Our results indicate that acute heroin substitution induces a subjective rewarding effect via increased striatal connectivity in heroin-dependent patients, suggesting that positive reinforcement effects in the striatum still occur after protracted maintenance therapy.

SUBMITTER: Schmidt A

PROVIDER: S-EPMC4354356 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Increased functional connectivity in the resting-state basal ganglia network after acute heroin substitution.

Schmidt A A Denier N N Magon S S Radue E-W EW Huber C G CG Riecher-Rossler A A Wiesbeck G A GA Lang U E UE Borgwardt S S Walter M M

Translational psychiatry 20150324

Reinforcement signals in the striatum are known to be crucial for mediating the subjective rewarding effects of acute drug intake. It is proposed that these effects may be more involved in early phases of drug addiction, whereas negative reinforcement effects may occur more in later stages of the illness. This study used resting-state functional magnetic resonance imaging to explore whether acute heroin substitution also induced positive reinforcement effects in striatal brain regions of protrac ...[more]

PMID: 25803496

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Project description:BACKGROUND: In the absence of overt stimuli, the brain shows correlated fluctuations in functionally related brain regions. Approximately ten largely independent resting state networks (RSNs) showing this behaviour have been documented to date. Recent studies have reported the existence of an RSN in the basal ganglia - albeit inconsistently and without the means to interpret its function. Using two large study groups with different resting state conditions and MR protocols, the reproducibility of the network across subjects, behavioural conditions and acquisition parameters is assessed. Independent Component Analysis (ICA), combined with novel analyses of temporal features, is applied to establish the basis of signal fluctuations in the network and its relation to other RSNs. Reference to prior probabilistic diffusion tractography work is used to identify the basal ganglia circuit to which these fluctuations correspond. RESULTS: An RSN is identified in the basal ganglia and thalamus, comprising the pallidum, putamen, subthalamic nucleus and substantia nigra, with a projection also to the supplementary motor area. Participating nuclei and thalamo-cortical connection probabilities allow this network to be identified as the motor control circuit of the basal ganglia. The network was reproducibly identified across subjects, behavioural conditions (fixation, eyes closed), field strength and echo-planar imaging parameters. It shows a frequency peak at 0.025 +/- 0.007 Hz and is most similar in spectral composition to the Default Mode (DM), a network of regions that is more active at rest than during task processing. Frequency features allow the network to be classified as an RSN rather than a physiological artefact. Fluctuations in this RSN are correlated with those in the task-positive fronto-parietal network and anticorrelated with those in the DM, whose hemodynamic response it anticipates. CONCLUSION: Although the basal ganglia RSN has not been reported in most ICA-based studies using a similar methodology, we demonstrate that it is reproducible across subjects, common resting state conditions and imaging parameters, and show that it corresponds with the motor control circuit. This characterisation of the basal ganglia network opens a potential means to investigate the motor-related neuropathologies in which the basal ganglia are involved.

Project description:BackgroundMusician's dystonia critically impacts professional musicians' careers as they may lose musical skills, which have been acquired through long and intensive training. Yet the pathophysiology of musician's dystonia and its link to the neural mechanisms supporting musical skills is poorly understood. We tested if resting-state functional connectivity might reflect an aspect of musical skill linked to the pathophysiology of musician's dystonia. We also tested a second hypothesis that the region with altered resting-state functional connectivity might be correlated with a quantitative measure of musical skills.MethodsWe studied 21 patients with musician's dystonia affecting their hands and 34 healthy musicians, using resting-state functional magnetic resonance imaging and behavioral assessment. We tested between-group differences of resting-state functional connectivity throughout the whole brain using independent component analysis.ResultsWe found abnormal basal ganglia resting-state functional connectivity in the putamina of patients with musician's dystonia compared with those of healthy musicians (P = 0.035 corrected for multiple comparisons). We also found that the temporal precision of keystrokes was correlated with basal ganglia functional connectivity in the putamina of healthy pianists (r = 0.72, P = 0.0005), but not in pianists with musician's dystonia (r = -0.11, P = 0.64).ConclusionsWe show that abnormalities of the putamen exist even at rest in musician's dystonia, whereas putaminal abnormality has previously been reported during a task. Moreover, basal ganglia resting-state functional connectivity in the putamen represented training levels in healthy musicians, and its disruption was associated with musician's dystonia. This novel finding hints at the pathophysiological mechanisms by which musician's dystonia follows extensive musical training. © 2018 The Authors. Movement Disorders published by Wiley Periodicals, Inc. on behalf of International Parkinson and Movement Disorder Society.

Dataset Information

Increased functional connectivity in the resting-state basal ganglia network after acute heroin substitution.

Publications

Increased functional connectivity in the resting-state basal ganglia network after acute heroin substitution.

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