The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion

121

Hcrt gene inactivation in mice leads to behavioral state instability, abnormal transitions to paradoxical sleep, and cataplexy, hallmarks of narcolepsy. Sleep homeostasis is, however, considered unimpaired in patients and narcoleptic mice. We find that whereas Hcrt ko/ko mice respond to 6-h sleep deprivation (SD) with a slowwave sleep (SWS) EEG δ (1.0 to 4.0 Hz) power rebound like WT littermates, spontaneous waking fails to induce a δ power reflecting prior waking duration. This correlates with impaired θ (6.0 to 9.5 Hz) and fast-γ (55 to 80 Hz) activity in prior waking. We algorithmically identify a theta-dominated wakefulness (TDW) substate underlying motivated behaviors and typically preceding cataplexy in Hcrt ko/ko mice. Hcrt ko/ko mice fully implement TDW when waking is enforced, but spontaneous TDW episode duration is greatly reduced. A reformulation of the classic sleep homeostasis model, where homeostatic pressure rises exclusively in TDW rather than all waking, predicts δ power dynamics both in Hcrt ko/ko and WT mouse baseline and recovery SWS. The low homeostatic impact of Hcrt ko/ko mouse spontaneous waking correlates with decreased cortical expression of neuronal activityrelated genes (notably Bdnf, Egr1/Zif268, and Per2). Thus, spontaneous TDW stability relies on Hcrt to sustain θ/fast-γ network activity and associated plasticity, whereas other arousal circuits sustain TDW during SD. We propose that TDW identifies a discrete global brain activity mode that is regulated by contextdependent neuromodulators and acts as a major driver of sleep homeostasis. Hcrt loss in Hcrt ko/ko mice causes impaired TDW maintenance in baseline wake and blunted δ power in SWS, reproducing, respectively, narcolepsy excessive daytime sleepiness and poor sleep quality.hypocretin/orexin | narcolepsy | sleep homeostasis | brain theta oscillations | waking substate W akefulness encompasses a wide spectrum of arousal levels, sensorimotor processing modes, and behaviors, reflected in the electroencephalogram (EEG) by a great variety of signal patterns (1). Fourier transform decomposes the signal into multiple frequency ranges, defining δ, θ (5 to 10 Hz), and γ (>30 Hz) oscillatory components. However, although the EEG has been used to define wakefulness and distinguish it from slow-wave and paradoxical sleep (SWS and PS) for decades, a formal cartography of waking substates, associated EEG features, and their significance for the animal is largely lacking. Likewise, definition of the relation between waking quality and subsequent sleep content has evolved little since enunciation of the twoprocess model of sleep regulation (2) in which a sleep/wakedependent homeostatic "process S," reflected in EEG δ power during SWS, regulates sleep propensity as a function of prior waking duration regardless of waking quality. Later studies described behaviors (3, 4) or EEG components (5, 6) that disproportionally affect the sleep homeostat. Different procedural, cognitive, or emotional experience differentially impacts subsequent SWS δ powe...

Section: Hcrt Is An Essential Regulator Of the Eeg Determinants Of Spsupporting

confidence: 85%

Section: Hcrt Is An Essential Regulator Of the Eeg Determinants Of Spmentioning

confidence: 99%

Section: Hcrt Is An Essential Regulator Of the Eeg Determinants Of Spmentioning

confidence: 99%

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Hypocretin (orexin) is critical in sustaining theta/gamma-rich waking behaviors that drive sleep need

Vassalli

Franken

2017

121

“…3A). However, because it has been reported (27)(28)(29)(30) that the frequency of the exploratory theta oscillations increases with the speed of the animal, we investigated whether or not this occurred in our mice. Because of the limitations of conventional power spectra in terms of time/ frequency resolution, we calculated the Wavelet power spectrum (31) as a function of time ( Fig.…”

Section: Exploratory Theta Oscillations In Wild-type and Task-3 Ko Anmentioning

confidence: 99%

An unexpected role for TASK-3 potassium channels in network oscillations with implications for sleep mechanisms and anesthetic action

Pang¹,

Robledo²,

Carr³

et al. 2009

TASK channels are acid-sensitive and anesthetic-activated members of the family of two-pore-domain potassium channels. We have made the surprising discovery that the genetic ablation of TASK-3 channels eliminates a specific type of theta oscillation in the cortical electroencephalogram (EEG) resembling type II theta (4 -9 Hz), which is thought to be important in processing sensory stimuli before initiating motor activity. In contrast, ablation of TASK-1 channels has no effect on theta oscillations. Despite the absence of type II theta oscillations in the TASK-3 knockout (KO) mice, the related type I theta, which has certain neuronal pathways in common and is involved in exploratory behavior, is unaffected. In addition to the absence of type II theta oscillations, the TASK-3 KO animals show marked alterations in both anesthetic sensitivity and natural sleep behavior. Their sensitivity to halothane, a potent activator of TASK channels, is greatly reduced, whereas their sensitivity to cyclopropane, which does not activate TASK-3 channels, is unchanged. The TASK-3 KO animals exhibit a slower progression from their waking to sleeping states and, during their sleeping period, their sleep episodes as well as their REM theta oscillations are more fragmented. These results imply a previously unexpected role for TASK-3 channels in the cellular mechanisms underlying these behaviors and suggest that endogenous modulators of these channels may regulate theta oscillations.I f a sufficient number of neurons participate in network oscillations, then the local field potentials summate, and measurable voltage oscillations can be recorded in the electroencephalogram (EEG). These oscillations are observed over a wide range of frequencies and reflect the synchronous neuronal activity that occurs during a variety of different behaviors. For example, as animals explore their environments, as they learn and lay down memories, as they process sensory input, and as they sleep, characteristic oscillations occur in the ''theta'' range of frequencies (4-12 Hz) (1). These theta oscillations are often divided into two types (1-5): Type I, which occurs at slightly higher frequencies (6-12 Hz), and type II (also known as arousal theta), which occurs at the lower end of the range (4-9 Hz). Type I theta is associated with exploratory behavior, walking, running, and rearing, whereas type II theta is associated with immobility during the processing of sensory stimuli relevant to initiating, or intending to initiate, motor activity.The neuronal networks that generate these theta oscillations involve ascending pathways from the brainstem that project to the hypothalamus and then to the medial septum/diagonal band of Broca and the hippocampus (6-9). Where the true pacemaker is located is unclear, but the basic requirements for a neuron to oscillate are a depolarizing drive (such as a sodium current) together with a restoring drive, such as a repolarizing potassium current. Most computational models (10-12) include several different ionic currents, som...

“…Both the power (1,3) and frequency (3)(4)(5)(6) of theta are positively correlated with running speed. Theta oscillations might therefore encode self-motion information and contribute to the generation of spatially modulated firing patterns (7)(8)(9).…”

mentioning

confidence: 95%

Human hippocampal theta power indicates movement onset and distance travelled

Bush

Bisby

Bird

et al. 2017

Theta frequency oscillations in the 6-to 10-Hz range dominate the rodent hippocampal local field potential during translational movement, suggesting that theta encodes self-motion. Increases in theta power have also been identified in the human hippocampus during both real and virtual movement but appear as transient bursts in distinct high-and low-frequency bands, and it is not yet clear how these bursts relate to the sustained oscillation observed in rodents. Here, we examine depth electrode recordings from the temporal lobe of 13 presurgical epilepsy patients performing a selfpaced spatial memory task in a virtual environment. In contrast to previous studies, we focus on movement-onset periods that incorporate both initial acceleration and an immediately preceding stationary interval associated with prominent theta oscillations in the rodent hippocampal formation. We demonstrate that movementonset periods are associated with a significant increase in both low (2-5 Hz)-and high (6-9 Hz)-frequency theta power in the human hippocampus. Similar increases in low-and high-frequency theta power are seen across lateral temporal lobe recording sites and persist throughout the remainder of movement in both regions. In addition, we show that movement-related theta power is greater both before and during longer paths, directly implicating human hippocampal theta in the encoding of translational movement. These findings strengthen the connection between studies of theta-band activity in rodents and humans and offer additional insight into the neural mechanisms of spatial navigation.theta | hippocampus | navigation | spatial memory | intracranial EEG T he rodent hippocampal local field potential (LFP) is dominated by 6-to 10-Hz theta oscillations during translational movement (1, 2). Both the power (1, 3) and frequency (3-6) of theta are positively correlated with running speed. Theta oscillations might therefore encode self-motion information and contribute to the generation of spatially modulated firing patterns (7-9). A critical concern for contemporary neuroscience is to establish whether this hypothesis can be translated across species. During navigation, intracranial recordings from depth electrodes in the human hippocampus have shown that theta is more prevalent during movement than during stationary periods (10-12) and that theta power increases with movement speed (13). In addition, increases in movement-related theta power are seen across the neocortex (10,11,14). These findings support the hypothesis that human theta oscillations might encode self-motion information. However, it has also been demonstrated that human theta-band activity typically occurs in transient bursts distributed throughout movement, in contrast to the continuous high-amplitude oscillation observed in the rodent (15,16). Moreover, these studies identified movement-related oscillations within both higher and lower frequency theta bands (17)(18)(19)(20). Hence, it is not yet clear how theta oscillations in the human hippocampus relate to thos...