Running speed and REM sleep control two distinct modes of rapid interhemispheric communication

Ghosh, Megha; Yang, Fang-Chi; Rice, Sharena P; Hetrick, Vaughn L.; Gonzalez, Alcides Lorenzo; Siu, Danny; Brennan, Ellen; John, Tibin T.; Ahrens, Allison M.; Ahmed, Omar J.

doi:10.1016/j.celrep.2022.111028

Cited by 10 publications

(7 citation statements)

References 133 publications

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“…Hence, the claustrum—a well-described 44 , 49 but functionally poorly understood area of the telencephalon—seems to have a role in SW sleep in reptiles and mammals 21 , 50 , and reflects competitive brain dynamics during REM P sleep (this paper), with origins in the midbrain. Antiphase activity between the two hemispheres has been identified in running rodents and during REM with fast rhythms (140-Hz ‘splines’) in superficial retrosplenial cortex 6 , but the mechanisms that underlie this relationship are unknown. The relative simplicity of the reptilian model may thus help to reveal not only some mechanisms of sleep, but also some of the functions of the claustrum and of the midbrain in sleep.…”

Section: Discussionmentioning

confidence: 99%

“…Our understanding of the functions and mechanisms of sleep remains incomplete, reflecting their increasingly evident complexity [1][2][3] . Likewise, studies of interhemispheric coordination during sleep [4][5][6] are often hard to connect precisely to known sleep circuits and mechanisms. Here, by recording from the claustra of sleeping bearded dragons (Pogona vitticeps), we show that, although the onsets and offsets of Pogona rapid-eye-movement (REM P ) and slow-wave sleep are coordinated bilaterally, these two sleep states differ markedly in their inter-claustral coordination.…”

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confidence: 99%

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Interhemispheric competition during sleep

Fenk

Riquelme

Laurent

2023

Nature

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Our understanding of the functions and mechanisms of sleep remains incomplete, reflecting their increasingly evident complexity1–3. Likewise, studies of interhemispheric coordination during sleep4–6 are often hard to connect precisely to known sleep circuits and mechanisms. Here, by recording from the claustra of sleeping bearded dragons (Pogona vitticeps), we show that, although the onsets and offsets of Pogona rapid-eye-movement (REMP) and slow-wave sleep are coordinated bilaterally, these two sleep states differ markedly in their inter-claustral coordination. During slow-wave sleep, the claustra produce sharp-wave ripples independently of one another, showing no coordination. By contrast, during REMP sleep, the potentials produced by the two claustra are precisely coordinated in amplitude and time. These signals, however, are not synchronous: one side leads the other by about 20 ms, with the leading side switching typically once per REMP episode or in between successive episodes. The leading claustrum expresses the stronger activity, suggesting bilateral competition. This competition does not occur directly between the two claustra or telencephalic hemispheres. Rather, it occurs in the midbrain and depends on the integrity of a GABAergic (γ-aminobutyric-acid-producing) nucleus of the isthmic complex, which exists in all vertebrates and is known in birds to underlie bottom-up attention and gaze control. These results reveal that a winner-take-all-type competition exists between the two sides of the brain of Pogona, which originates in the midbrain and has precise consequences for claustrum activity and coordination during REMP sleep.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Interhemispheric competition during sleep

Fenk

Riquelme

Laurent

2023

Nature

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“…How does the lack of cholinergically-induced persistent firing impact LR coding of AHV? Cholinergic release in retrosplenial cortex ramps up dramatically during states of navigation-related locomotion (increased linear speed) compared to states with no linear motion ( Anzalone et al, 2009 ), accompanied by precise changes in theta-coupled gamma and spline rhythms in RSG ( Alexander et al, 2018 ; Ghosh et al, 2022 ). However, animals can rotate their heads when their bodies are otherwise still (zero linear speed, with low cholinergic levels) and also when locomoting (high linear speed, with high cholinergic levels; Anzalone et al, 2009 ).…”

Section: Discussionmentioning

confidence: 99%

Cell-type-specific cholinergic control of granular retrosplenial cortex with implications for angular velocity coding across brain states

Jedrasiak-Cape,

Rybicki-Kler,

Brooks

et al. 2024

Preprint

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Cholinergic receptor activation enables the persistent firing of cortical pyramidal neurons, providing a key cellular basis for theories of spatial navigation involving working memory, path integration, and head direction encoding. The granular retrosplenial cortex (RSG) is important for spatially-guided behaviors, but how acetylcholine impacts RSG neurons is unknown. Here, we show that a transcriptomically, morphologically, and biophysically distinct RSG cell-type – the low-rheobase (LR) neuron – has a very distinct expression profile of cholinergic muscarinic receptors compared to all other neighboring excitatory neuronal subtypes. LR neurons do not fire persistently in response to cholinergic agonists, in stark contrast to all other principal neuronal subtypes examined within the RSG and across midline cortex. This lack of persistence allows LR neuron models to rapidly compute angular head velocity (AHV), independent of cholinergic changes seen during navigation. Thus, LR neurons can consistently compute AHV across brain states, highlighting the specialized RSG neural codes supporting navigation.

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“…In addition, for a value to be identified as a peak, the preceding and subsequent values needed to be at least 1 SD (derived from baseline data) below the peak value. These parameters were adopted from peak analyses in neurophysiological studies (e.g., Ghosh et al, 2022) and ensured a robust separation of peaks from potentially noisy recordings of relatively small currents.…”

Section: Chronic Implantation Of Microelectrode Arrays (Meas)mentioning

confidence: 99%

Cortico-striatal action control inherent of opponent cognitive-motivational styles

Avila,

Sarter

2024

Preprint

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Turning on cue or stopping at a red light requires the detection of such cues to select action sequences, or suppress action, in accordance with cue-associated action rules. Cortico-striatal projections are an essential part of the neuronal attention-motor interface. Here, we used glutamate-sensing microelectrode arrays to measure glutamate transients in the dorsomedial striatum (DMS) of male and female rats walking a treadmill and executing cued turns and stops. Prelimbic-DMS projections were chemogenetically inhibited to determine their behavioral necessity and the cortico-striatal origin of cue-evoked glutamate transients. Furthermore, we investigated rats exhibiting preferably goal-directed (goal trackers, GTs) versus cue-driven attention (sign trackers, STs), to determine the impact of such cognitive-motivational biases on cortico-striatal control. GTs executed more cued turns, and initiated such turns more slowly, than STs. During turns, but not missed turns or cued stops, cue-evoked glutamate concentrations were higher in GTs than in STs. In conjunction with turn cue-evoked glutamate spike levels, the presence of a single spike rendered GTs to be almost twice as likely to turn than STs. In contrast, multiple glutamate spikes predicted STs to be robustly more likely to turn than GTs. In GTs, inhibition of prelimbic-DMS projections attenuated turn rates and turn cue-evoked glutamate peaks and increased the number of spikes. These findings suggest that turn cue-evoked glutamate release dynamics in GTs are tightly controlled by cortico-striatal neuronal activity. In contrast, in STs, glutamate release from DMS glutamatergic terminals is regulated by other striatal circuitry, preferably mediating cued suppression of action and reward tracking.

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Running speed and REM sleep control two distinct modes of rapid interhemispheric communication

Cited by 10 publications

References 133 publications

Interhemispheric competition during sleep

Interhemispheric competition during sleep

Cell-type-specific cholinergic control of granular retrosplenial cortex with implications for angular velocity coding across brain states

Cortico-striatal action control inherent of opponent cognitive-motivational styles

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