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Circadian and Homeostatic Modulation of Multi-Unit Activity in Midbrain Dopaminergic Structures Received: 12 January 2018 Karim Fifel 1,2, Johanna H

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Circadian and Homeostatic Modulation of Multi-Unit Activity in Midbrain Dopaminergic Structures Received: 12 January 2018 Karim Fifel 1,2, Johanna H www.nature.com/scientificreports OPEN Circadian and Homeostatic Modulation of Multi-Unit Activity in Midbrain Dopaminergic Structures Received: 12 January 2018 Karim Fifel 1,2, Johanna H. Meijer1 & Tom Deboer1 Accepted: 24 April 2018 Although the link between sleep disturbances and dopamine (DA)-related neurological and Published: xx xx xxxx neuropsychiatric disorders is well established, the impact of sleep alterations on neuronal activity of midbrain DA-ergic structures is currently unknown. Here, using wildtype C57Bl mice, we investigated the circadian- and sleep-related modulation of electrical neuronal activity in midbrain ventral- tegmental-area (VTA) and substantia nigra (SN). We found no signifcant circadian modulation of activity in SN while VTA displayed a low amplitude but signifcant circadian modulation with increased fring rates during the active phase. Combining neural activity recordings with electroencephalogram (EEG) recordings revealed a strong vigilance state dependent modulation of neuronal activity with increased activity during wakefulness and rapid eye movement sleep relative to non-rapid eye movement sleep in both SN and VTA. Six-hours of sleep deprivation induced a signifcant depression of neuronal activity in both areas. Surprisingly, these alterations lasted for up to 48 hours and persisted even after the normalization of cortical EEG waves. Our results show that sleep and sleep disturbances signifcantly afect neuronal activity in midbrain DA structures. We propose that these changes in neuronal activity underlie the well-known relationship between sleep alterations and several disorders involving dysfunction of the DA circuitry such as addiction and depression. Located in the mesencephalon, the ventral tegmental area (VTA) and Substantia nigra (SN) are the main sources of dopamine (DA) in the basal ganglia and forebrain1. Within these structures dopaminergic (70%), GABAergic (30%) and glutamatergic (2–3% only in the VTA) neurons are anatomically intermingled and electrophysio- logically connected2. Functionally, these clusters of neurochemically diverse neurons control and/or modulate a broad range of behaviors including goal-directed behavior, motor actions, motivation, response to reward, learning, working memory, attention and decision-making3. Recently, growing interest has been shown towards the investigation of the role of VTA- and SN-dopaminergic and GABAergic neurons in the regulation of sleep and wakefulness4–9. Tis interest has been partially sparked by the recognition of sleep/wake cycle alterations in many neurological disorders in which VTA and SN function, including DA release, is compromised, such as Parkinson’s disease (PD)10,11. Inversely, alterations of the sleep-wake cycle are associated with risks for a wide variety of medi- cal conditions directly or indirectly modulated by DA neurocircuitry12–15. Sleep deprivation (SD) adversely afects cognitive performances16, impairs judgment and decision making16, biases values computations by increasing the emphasis on gain outcomes relative to losses17–21, intensifes drug abuse and increases the likelihood of relapse afer withdrawal22,23. Recent animal studies as well as imaging studies in humans have shown that SD produces aberrant function- ing in multiple sites of the dopaminergic reward circuitry and that these alterations were signifcantly correlated with SD-related behavioral and functional alterations17–21. Moreover, the modulation of the DA neurotransmis- sion has been implicated in the therapeutic efects of SD in major depression24 as well as in the motor benefts experienced by a subset of patients with PD25. The sensitivity of different brain structures to SD is variable26–28 suggesting that some brain structures belonging to the reward neuronal network might be more responsive to SD than others. Although some of the brain areas afected by SD are part of the DA circuitry26–28, the underlying mechanism(s) by which SD afects the 1Department of Molecular Cell Biology, Neurophysiology unit, Leiden University Medical Center, P.O. Box 9600, 2300 RC, Leiden, The Netherlands. 2Present address: International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305–8575, Japan. Correspondence and requests for materials should be addressed to K.F. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:7765 | DOI:10.1038/s41598-018-25770-5 1 www.nature.com/scientificreports/ mesocorticolimbic reward circuitry remain poorly understood. Additionally, whether sleep loss afects the elec- trophysiology of midbrain VTA and SN structures is unknown. We therefore set out to assess the acute and long-term efects of a 6-hour sleep deprivation on electrical impulse frequency, also called multi-unit activity (MUA), as a measure of activity of neurons in the VTA and SN. In addition, electroencephalogram (EEG) and electromyogram (EMG) recordings were performed to investigate changes in the characteristics of sleep and waking before, during and afer SD and their correlation with neuronal activity in VTA and SN. Given that SD afects DA neurotransmission29, we hypothesize that SD will alter the electrical activity of these midbrain structures. Materials and Methods Animals and locomotor activity recordings. Te experiments were performed in rooms with monitored constant temperature and humidity conditions. Food and water were available ad libitum. A total of 17 adult male C57Bl/6JOlaHsd mice (16–20 weeks age old at the time of experiments) were used for this study. Te animals were purchased from Harlan (Te Netherlands). All the experiments were approved by of the Ethics Committee of Leiden University Medical Center and were carried out in accordance with the EU Directive 2010/63/EU on the protection of animals used for scientifc purposes. Animal cages were equipped with passive infrared motion sensors to record general locomotor activity. In vivo multi-unit activity, EEG, and EMG recordings. In vivo multiunit activity (MUA) and EEG and EMG were recorded as described previously30. In brief, for the MUA recordings, stainless steel tripolar electrodes (0.125 mm diameter; Plastics One, Inc., Roanoke, VA) were implanted in each animal under deep anaesthesia. For diferential recordings, two electrodes were directed toward the targeted midbrain structure with 0.4-mm space between the electrodes. Te third electrode was placed in the cortex as a reference electrode. Measurements were performed from one electrode at a time. Te electrodes were placed to record from the ventral tegmental area (VTA, relative to Bregma: 3.16 mm posterior and 0.59 mm lateral; depth: 4.37 mm), medial substantia nigra (SNM, relative to Bregma: 3.16 mm posterior and 1.11 mm lateral; depth: 4.22 mm) and lateral substantia nigra (SNL, relative to Bregma: 3.16 mm posterior and 1.75 mm lateral; depth: 3.7 mm). Te coordinates were adapted from ref.31 (Supplemental Fig. S1). For EEG, electrodes were screwed into the skull above the dura over the right cortex (2.0 mm lateral to the midline and 3.5 mm posterior to Bregma) and cerebellum (at the midline and 1.5 mm posterior to lambda). For EMG recordings, two wires with suture patches were inserted in the tissue between the skin and the neck muscle. Te animals were connected to the recording system via a fexible cable and counterbalanced swivel system, and the animals were acclimated to the setup under similar (12:12 L:D, food ad libitum) conditions. Te animals’ behavioural activity (drinking and locomotion) was recorded continuously in order to obtain an estimate of the circadian rhythm. Neuronal activity in the midbrain structures was amplifed approximately 40,000X, band-pass fltered (500– 5,000 Hz, −40 dB/decade). Online, a window discriminator converted the action potentials into electronic pulses. A second window discriminator was set at a higher level to detect artefacts caused by the animal’s movements. Action potentials and movement-related artefacts were counted in 10-s epochs. Te analogue EEG and EMG signals, which were recorded continuously, were amplifed approximately 2,000X, band-pass fltered (0.5–30 Hz, −40 dB/decade), and digitized at 100 Hz. All data were recorded simultaneously and stored on a computer hard disk. Te stability of the multi-unit signal and EEG recording was evaluated daily by visually inspecting the sig- nals. Te circadian rhythm in the signal and the amplitude of the EEG were monitored before the baseline data were collected. As soon as the signals were stable, experimental recordings were started. Afer the experiments, the animals were sacrifced to verify the recording sites. To mark the location of the electrode tip, current was passed through the electrode, and the brain was perfused with a bufered solution containing 4% paraformalde- hyde and 8% potassium ferrocyanide. Te brains were removed, post-fxed overnight in 4% paraformaldehyde, and cryo-protected in 30% sucrose solution. Free-foating coronal sections (40 μm thickness) were cut on a freezing microtome. Te sections were stained with cresyl violet, mounted on gelatinized slides, dried, dehydrated in increasing gradients of ethanol, cleared in toluene, and cover-slipped with Depex. Ofine, the EEG power density spectra were calculated in 10-s epochs corresponding to the 10-s epochs of the action potentials of the targeted hypothalamic structure using a fast Fourier transform (FFT) routine within the frequency range of 0–25.0 Hz in 0.1-Hz bins. EMG signals were integrated over 10-s epochs. Tree
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