Pedunculopontine Nucleus Gamma Band Activity-Preconscious Awareness, Waking, and REM Sleep

Urbano, Francisco J.; D’Onofrio, Stasia; Luster, Brennon; Beck, Paige; Hyde, James; Bisagno, Verónica; García‐Rill, Edgar

doi:10.3389/fneur.2014.00210

Cited by 33 publications

(55 citation statements)

References 105 publications

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“…Indeed, unlike immobility, in both animal and human, locomotion engages the subject to move and interact in its environment and is potentially risky or unstable because unexpected deleterious events can happen. The sensory-gating provided by RAS may be necessary during locomotion (Garcia-Rill 1991) as it would allow to process preconsciously large amounts of information in a moving environement (Urbano et al 2014). Then, the RAS including the MRF neurons would further modulate higher-level beta/gamma processing through its ascending projections .…”

Section: Mrf Neurons Involved In Wakingmentioning

confidence: 99%

The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state

et al. 2016

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The mesencephalic reticular formation (MRF) mainly composed by the pedunculopontine and the cuneiform nuclei is involved in the control of several fundamental brain functions such as locomotion, rapid eye movement sleep and waking state. On the one hand, the role of MRF neurons in locomotion has been investigated for decades in different animal models, including in behaving nonhuman primate (NHP) using extracellular recordings. On the other hand, MRF neurons involved in the control of waking state have been consistently shown to constitute the cholinergic component of the reticular ascending system. However, a dual control of the locomotion and waking state by the same groups of neurons in NHP has never been demonstrated in NHP. Here, using microelectrode recordings in behaving NHP, we recorded 38 neurons in the MRF that were followed during transition between wakefulness (TWS) and sleep, i.e., until the emergence of sleep episodes characterized by typical cortical slow wave activity (SWA). We found that the MRF neurons, mainly located in the pedunculopontine nucleus region, modulated their activity during TWS with a decrease in firing rate during SWA. Of interest, we could follow some MRF neurons from locomotion to SWA and found that they also modulated their firing rate during locomotion and TWS. These new findings confirm the role of MRF neurons in both functions. They suggest that the MRF is an integration center that potentially allows to fine tune waking state and locomotor signals in order to establish an efficient locomotion.

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Section: Mrf Neurons Involved In Wakingmentioning

confidence: 99%

The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state

et al. 2016

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“…Moreover, during REM sleep, pCREB activation in PPN cholinergic neurons was induced by REM sleep, and PPN intracellular PKA activation is mediated by a transcriptional cascade involving pCREB (Datta et al 2009). These findings suggest that waking in vivo may be modulated by the CaMKII pathway while REM sleep may be modulated by the cAMP/PKA pathway in the PPN (Garcia-Rill et al 2014; Urbano et al 2014). In addition, it appears that the cAMP-dependent pathway phosphorylates N-type calcium channels (Hell et al 1995), while CaMKII regulates P/Q-type calcium channels (Jenkins et al 2005).…”

Section: Two Pathways Two Statesmentioning

confidence: 87%

“…In addition, it appears that the cAMP-dependent pathway phosphorylates N-type calcium channels (Hell et al 1995), while CaMKII regulates P/Q-type calcium channels (Jenkins et al 2005). Therefore, the presence of P/Q-type calcium channels is related to CaMKII and waking, while the presence of N-type calcium channels is more related to cAMP and REM sleep (Garcia-Rill et al 2014; Urbano et al 2014). …”

Section: Two Pathways Two Statesmentioning

confidence: 99%

“…The following review describes the latest findings on PPN physiology that suggest that, a) two different intracellular pathways control gamma band activity during waking compared to REM sleep, b) these two pathways differentially control the two different types of high threshold voltage-dependent calcium channels (N- and P/Q-type), c) there are separate populations of PPN cells bearing one or both channels, d) this organization informs regarding the mechanisms behind the developmental decrease in REM sleep, and e) such findings have implications for the mechanisms behind insomnia, as well as schizophrenia and bipolar disorder. The PPN, as part of the reticular activating system (RAS) and its role in generating gamma band activity suggest its participation in arousal and preconscious awareness (Garcia-Rill et al 2014; Urbano et al 2014), therefore, it is not surprising that it is involved in all of these disorders.…”

Section: Introductionmentioning

confidence: 99%

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Implications of gamma band activity in the pedunculopontine nucleus

et al. 2015

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The fact that the pedunculopontine nucleus (PPN) is part of the reticular activating system places it in a unique position to modulate sensory input and fight-or-flight responses. Arousing stimuli simultaneously activate ascending projections of the PPN to the intralaminar thalamus to trigger cortical high frequency activity and arousal, as well as descending projections to reticulospinal systems to alter posture and locomotion. As such, the PPN has become a target for deep brain stimulation (DBS) for the treatment of Parkinson’s disease (PD), modulating gait, posture, and higher functions. This article describes the latest discoveries on PPN physiology and the role of the PPN in a number of disorders. It has now been determined that high frequency activity during waking and REM sleep is controlled by two different intracellular pathways and two calcium channels in PPN cells. Moreover, there are three different PPN cell types that have one or both calcium channels and may be active during waking only, REM sleep only, or both. Based on the new discoveries, novel mechanisms are proposed for insomnia as a waking disorder. In addition, neuronal calcium sensor protein-1 (NCS-1), which is over expressed in schizophrenia and bipolar disorder, may be responsible for the dysregulation in gamma band activity in at least some patients with these diseases. Recent results suggest that NCS-1 modulates PPN gamma band activity and that lithium acts to reduce the effects of over expressed NCS-1, accounting for its effectiveness in bipolar disorder.

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“…Moreover, based on a number of the animal studies [50][51][52], the PPT has become the main target for deep brain stimulation for the treatment of movement and postural disorders in humans [53]. PPT as the main brain source of thalamocortical cholinergic innervation has an important functions relevant to the regulation of REM sleep [54,55], arousal [55,56], and various motor control systems [53,57], including breathing control [58][59][60]. In addition, in relation to motor and cognitive function control, particularly in relation to Parkinson's disease, the PPT is postulated as an important interface between the basal ganglia and cerebellum [61].…”

Section: Transl Brainmentioning

confidence: 99%

Sleep spindles as an early biomarker of REM sleep disorder in a rat model of Parkinson’s disease cholinopathy

Ciric¹,

Lazic²,

Petrović³

et al. 2017

Transl Brain Rhythmicity

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Rhythmic oscillations of neuronal populations, generated by different mechanisms, are present at several levels of the central nervous system and serve many important physiological or reflect pathological functions. Understanding the role of brain oscillations as possible biomarkers of brain function and plasticity is still a challenge, and despite extensive research, their role is still not well established.We recently demonstrated that the hallmarks of earlier aging onset during impaired thalamo-cortical cholinergic innervation (in a rat model of Parkinson's disease cholinopathy) were consistently expressed, from 3 and one half to 5 and one half months of age, through increased electroencephalographic (EEG) sigma activity amplitude during rapid eye movement (REM) sleep, as a unique aging induced REM sleep phenomenon. In addition, there was altered motor cortical drive during non-rapid-eye-movement (NREM) and REM sleep.In order to explain this new aging-induced REM sleep phenomenon, we analyzed possible differences between control REM sleep spindle activity and REM sleep spindle activity at the onset of REM sleep "enriched" with sigma activity (at 4 and one half months of age), following bilateral pedunculopontine tegmental nucleus (PPT) cholinergic neuronal loss in the rat. We analzyed differences in spindle density, duration, and frequency.We demonstrated in young adult Wistar rats with the severely impaired PPT cholinergic innervation the alterations in sleep spindle dynamics and pattern during REM sleep in the motor cortex as the earliest biomarkers for the onset of their altered aging processes.

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Pedunculopontine Nucleus Gamma Band Activity-Preconscious Awareness, Waking, and REM Sleep

Cited by 33 publications

References 105 publications

The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state

The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state

Implications of gamma band activity in the pedunculopontine nucleus

Sleep spindles as an early biomarker of REM sleep disorder in a rat model of Parkinson’s disease cholinopathy

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