Decreased brain connectivity in smoking contrasts with increased connectivity in drinking
- Fudan University, China
- University of Cambridge, United Kingdom
- Xidian University, China
- Shanghai University Finance and Economics, China
- University of Warwick, United Kingdom
- Beijing Institute of Genomics, Chinese Academy of Sciences, China
- King's College London, United Kingdom
- University of Vermont, United States
- University Paris Descartes, France
- Université Paris-Saclay, France
- Technische Universität Dresden, Germany
- University of Electronic Science and Technology of China, China
Abstract
In a group of 831 participants from the general population in the Human Connectome Project, smokers exhibited low overall functional connectivity, and more specifically of the lateral orbitofrontal cortex which is associated with non-reward mechanisms, the adjacent inferior frontal gyrus, and the precuneus. Participants who drank a high amount had overall increases in resting state functional connectivity, and specific increases in reward-related systems including the medial orbitofrontal cortex and the cingulate cortex. Increased impulsivity was found in smokers, associated with decreased functional connectivity of the non-reward-related lateral orbitofrontal cortex; and increased impulsivity was found in high amount drinkers, associated with increased functional connectivity of the reward-related medial orbitofrontal cortex. The main findings were cross-validated in an independent longitudinal dataset with 1176 participants, IMAGEN. Further, the functional connectivities in 14-year-old non-smokers (and also in female low-drinkers) were related to who would smoke or drink at age 19. An implication is that these differences in brain functional connectivities play a role in smoking and drinking, together with other factors.
Data availability
The dataset used in this study and custom code is available at Dryad.
-
Data from: Decreased brain connectivity in smoking contrasts with increased connectivity in drinkingDryad Digital Repository, doi.org/10.5061/dryad.736t01r.
Article and author information
Author details
Dimitri Papadopoulos Orfanos
Funding
National Natural Science Foundation of China (71661167002)
- Jianfeng Feng
The Key Project of Shanghai Science & Technology Innovation Plan (16JC1420402)
- Jianfeng Feng
National Natural Science Foundation of China (81701773)
- Wei Cheng
Shanghai Sailing Program (17YF1426200)
- Wei Cheng
Natural Science Foundation of Shanghai (18ZR1404400)
- Wei Cheng
The Key Project of Shanghai Science & Technology Innovation Plan (15JC1400101)
- Jianfeng Feng
The Shanghai AI Platform for Diagnosis and Treatment of Brain Diseases (2016-17)
- Jianfeng Feng
Base for Introducing Talents of Discipline to Universities (B18015)
- Jianfeng Feng
National Natural Science Foundation of China (91630314)
- Jianfeng Feng
National Natural Science Foundation of China (11771010)
- Wei Cheng
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The WU-Minn HCP Consortium obtained full informed consent from all participants, and research procedures and ethical guidelines were followed in accordance with the Washington University Institutional Review Boards (IRB #201204036; Title: 'Mapping the Human Connectome: Structure, Function, and Heritability').
Copyright
© 2019, Cheng et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 5,576
- views
-
- 641
- downloads
-
- 45
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Decreased brain connectivity in smoking contrasts with increased connectivity in drinking
eLife 8:e40765.
https://doi.org/10.7554/eLife.40765
Further reading
-
- Neuroscience
Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.
-
- Neuroscience
The classical diagnosis of Parkinsonism is based on motor symptoms that are the consequence of nigrostriatal pathway dysfunction and reduced dopaminergic output. However, a decade prior to the emergence of motor issues, patients frequently experience non-motor symptoms, such as a reduced sense of smell (hyposmia). The cellular and molecular bases for these early defects remain enigmatic. To explore this, we developed a new collection of five fruit fly models of familial Parkinsonism and conducted single-cell RNA sequencing on young brains of these models. Interestingly, cholinergic projection neurons are the most vulnerable cells, and genes associated with presynaptic function are the most deregulated. Additional single nucleus sequencing of three specific brain regions of Parkinson’s disease patients confirms these findings. Indeed, the disturbances lead to early synaptic dysfunction, notably affecting cholinergic olfactory projection neurons crucial for olfactory function in flies. Correcting these defects specifically in olfactory cholinergic interneurons in flies or inducing cholinergic signaling in Parkinson mutant human induced dopaminergic neurons in vitro using nicotine, both rescue age-dependent dopaminergic neuron decline. Hence, our research uncovers that one of the earliest indicators of disease in five different models of familial Parkinsonism is synaptic dysfunction in higher-order cholinergic projection neurons and this contributes to the development of hyposmia. Furthermore, the shared pathways of synaptic failure in these cholinergic neurons ultimately contribute to dopaminergic dysfunction later in life.
