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Lesion of the pedunculopontine tegmental nucleus in rat augments cortical activation and disturbs sleep/wake state transitions structure.
Exp Neurol 2013; 247:562-71EN

Abstract

The pedunculopontine tegmental nucleus (PPT) represents a major aggregation of cholinergic neurons in the mammalian brainstem, which is important in the generation and maintenance of REM sleep. We investigated the effects of unilateral and bilateral PPT lesions on sleep and all the conventional sleep-state related EEG frequency bands amplitudes, in an attempt to find the EEG markers for the onset and progression of PPT cholinergic neuronal degeneration. The experiments were performed on 35 adult male Wistar rats, chronically implanted for sleep recording. During the surgical procedure for EEG and EMG electrodes implantation, the unilateral or bilateral PPT lesion was produced under ketamine/diazepam anesthesia, by the stereotaxically guided microinfusion of 100 nl 0.1M ibotenic acid (IBO) into PPT. We applied Fourier analysis to signals acquired throughout 6h of recordings, and each 10s epoch was differentiated as a Wake, NREM or REM state. We also calculated the group probability density estimates (PDE) of all Wake, NREM and REM conventional EEG frequency amplitudes, and the number of all the transition states using MATLAB 6.5. Our results show that the unilateral or bilateral PPT lesions did not change the sleep/wake architecture, but did change the sleep/wake state transitions structure and the sleep/state related "EEG microstructure". Unilateral or bilateral PPT lesions sustainably increased Wake/REM and REM/Wake transitions from 14 to 35 days after lesions. This was followed by decreased NREM/REM and REM/NREM transitions from 28 days only in the case of the bilateral PPT lesion. The unilateral PPT lesion augmented both Wake theta and REM beta while it also attenuated the relative amplitude of the Wake delta frequency, with a delay of one week. Following a bilateral PPT lesion there was augmentation of the relative amplitude of the Wake, NREM, and REM beta and REM gamma frequency which occurred simultaneously to NREM and Wake delta attenuation. We have shown that the PPT cholinergic neuronal loss sustainably increased the number of the Wake/REM and REM/Wake transitions and augmented sleep-states related cortical activation that was simultaneously expressed by the high frequency amplitude augmentation, as well as Wake and NREM delta frequency attenuation.

Authors+Show Affiliations

University of Belgrade, Department of Neurobiology, Institute for Biological Research, Sinisa Stankovic, 11 060 Belgrade, Serbia.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

23481548

Citation

Petrovic, Jelena, et al. "Lesion of the Pedunculopontine Tegmental Nucleus in Rat Augments Cortical Activation and Disturbs Sleep/wake State Transitions Structure." Experimental Neurology, vol. 247, 2013, pp. 562-71.
Petrovic J, Ciric J, Lazic K, et al. Lesion of the pedunculopontine tegmental nucleus in rat augments cortical activation and disturbs sleep/wake state transitions structure. Exp Neurol. 2013;247:562-71.
Petrovic, J., Ciric, J., Lazic, K., Kalauzi, A., & Saponjic, J. (2013). Lesion of the pedunculopontine tegmental nucleus in rat augments cortical activation and disturbs sleep/wake state transitions structure. Experimental Neurology, 247, pp. 562-71. doi:10.1016/j.expneurol.2013.02.007.
Petrovic J, et al. Lesion of the Pedunculopontine Tegmental Nucleus in Rat Augments Cortical Activation and Disturbs Sleep/wake State Transitions Structure. Exp Neurol. 2013;247:562-71. PubMed PMID: 23481548.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Lesion of the pedunculopontine tegmental nucleus in rat augments cortical activation and disturbs sleep/wake state transitions structure. AU - Petrovic,Jelena, AU - Ciric,Jelena, AU - Lazic,Katarina, AU - Kalauzi,Aleksandar, AU - Saponjic,Jasna, Y1 - 2013/02/26/ PY - 2012/11/23/received PY - 2013/01/30/revised PY - 2013/02/13/accepted PY - 2013/3/14/entrez PY - 2013/3/14/pubmed PY - 2013/12/16/medline KW - Cholinergic neurons KW - Electroencephalography KW - Ibotenic acid KW - Lesion KW - Pedunculopontine tegmental nucleus KW - Rat KW - Sleep–wake states KW - Sleep–wake states transitions SP - 562 EP - 71 JF - Experimental neurology JO - Exp. Neurol. VL - 247 N2 - The pedunculopontine tegmental nucleus (PPT) represents a major aggregation of cholinergic neurons in the mammalian brainstem, which is important in the generation and maintenance of REM sleep. We investigated the effects of unilateral and bilateral PPT lesions on sleep and all the conventional sleep-state related EEG frequency bands amplitudes, in an attempt to find the EEG markers for the onset and progression of PPT cholinergic neuronal degeneration. The experiments were performed on 35 adult male Wistar rats, chronically implanted for sleep recording. During the surgical procedure for EEG and EMG electrodes implantation, the unilateral or bilateral PPT lesion was produced under ketamine/diazepam anesthesia, by the stereotaxically guided microinfusion of 100 nl 0.1M ibotenic acid (IBO) into PPT. We applied Fourier analysis to signals acquired throughout 6h of recordings, and each 10s epoch was differentiated as a Wake, NREM or REM state. We also calculated the group probability density estimates (PDE) of all Wake, NREM and REM conventional EEG frequency amplitudes, and the number of all the transition states using MATLAB 6.5. Our results show that the unilateral or bilateral PPT lesions did not change the sleep/wake architecture, but did change the sleep/wake state transitions structure and the sleep/state related "EEG microstructure". Unilateral or bilateral PPT lesions sustainably increased Wake/REM and REM/Wake transitions from 14 to 35 days after lesions. This was followed by decreased NREM/REM and REM/NREM transitions from 28 days only in the case of the bilateral PPT lesion. The unilateral PPT lesion augmented both Wake theta and REM beta while it also attenuated the relative amplitude of the Wake delta frequency, with a delay of one week. Following a bilateral PPT lesion there was augmentation of the relative amplitude of the Wake, NREM, and REM beta and REM gamma frequency which occurred simultaneously to NREM and Wake delta attenuation. We have shown that the PPT cholinergic neuronal loss sustainably increased the number of the Wake/REM and REM/Wake transitions and augmented sleep-states related cortical activation that was simultaneously expressed by the high frequency amplitude augmentation, as well as Wake and NREM delta frequency attenuation. SN - 1090-2430 UR - https://www.unboundmedicine.com/medline/citation/23481548/Lesion_of_the_pedunculopontine_tegmental_nucleus_in_rat_augments_cortical_activation_and_disturbs_sleep/wake_state_transitions_structure_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0014-4886(13)00060-5 DB - PRIME DP - Unbound Medicine ER -