Sleep as a window on the sensorimotor foundations of the developing hippocampus

Rio-Bermudez, Carlos Del; Blumberg, Mark S.

doi:10.1002/hipo.23334

Cited by 11 publications

(10 citation statements)

References 121 publications

(185 reference statements)

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“…Neural activity in these two areas was highest during movement-related periods of AS, but it was also higher during AS than wake even in the absence of movement, thus suggesting state-dependent modulation. Accordingly, the present findings add to the growing body of evidence that state-dependent modulation is a general feature of developing cortex (Mukherjee et al, 2017;Blumberg et al, 2020;Del Rio-Bermudez and Blumberg, 2022).…”

Section: Prefrontal Cortex Is Most Active During Sleepsupporting

confidence: 75%

Activity in developing prefrontal cortex is shaped by sleep and sensory experience

Gómez

Dooley

Blumberg

2022

Preprint

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In developing rats, behavioral state exerts a profound modulatory influence on neural activity throughout the sensorimotor system, including primary motor cortex (M1). We hypothesized that similar state-dependent modulation occurs in higher-order cortical areas with which M1 forms functional connections. Here, using 8- and 12-day-old rats cycling freely between sleep and wake, we record neural activity in M1, secondary motor cortex (M2), and medial prefrontal cortex (mPFC). At both ages in all three areas, neural activity increased during active sleep (AS) compared with wake. Regardless of behavioral state, neural activity in M2 and mPFC increased during periods when limbs were moving. This movement-related activity in M2 and mPFC, like that in M1, is driven by sensory feedback. Our results, which diverge from those of previous studies using anesthetized pups, demonstrate that AS-dependent modulation and sensory responsivity extend to prefrontal cortex. These findings expand the range of factors shaping the activity-dependent development of higher-order cortical areas.

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Section: Prefrontal Cortex Is Most Active During Sleepsupporting

confidence: 75%

Activity in developing prefrontal cortex is shaped by sleep and sensory experience

Gómez

Dooley

Blumberg

2022

Preprint

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“…This is a consistent finding in previous polysomnographic studies [ 12 , 40 ], revealing severe REM suppression in RTT. REM sleep is supposed to be engaged in brain development [ 58 , 59 ] and particularly sensorimotor development [ 60 ]; that is, newborns spend about half of their sleep time in REM sleep, which continues to decrease to about 20% in adulthood [ 61 ]. There is also mounting evidence that REM sleep primes early hippocampal sensorimotor networks towards emerging motor capacities later in life (see the work by Blumberg M. et al).…”

Section: Discussionmentioning

confidence: 99%

Literature Cases Summarized Based on Their Polysomnographic Findings in Rett Syndrome

Zhang

Spruyt

2022

IJERPH

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Rett syndrome (RTT) is a severe and rare neurodevelopmental disorder affecting mostly girls. In RTT, an impaired sleep pattern is a supportive criterion for the diagnosis, yet little is known regarding the sleep structure and sleep respiratory events. Aiming to delineate sleep by aggregating RTT case (series) data from published polysomnographic studies, seventy-four RTT cases were collected from eleven studies up until 6 February 2022 (PROSPERO: CRD 42020198099). We compared the polysomnographic data within RTT stratifications and to a typically developing population. MECP2 cases demonstrated shortened total sleep time (TST) with increased stage N3 and decreased REM sleep. In cases with CDKL5 mutations, TST was longer and they spent more time in stage N1 but less in stage N3 than those cases affected by MECP2 mutations and a typically developing population. Sleep-disordered breathing was confirmed by the abnormal apnea/hypopnea index of 11.92 ± 23.67/h TST in these aggregated cases. No association of sleep structure with chronological age was found. In RTT, the sleep macrostructure of MECP2 versus CDKL5 cases showed differences, particularly regarding sleep stage N3. A severe REM sleep propensity reduction was found. Aberrant sleep cycling, possibly characterized by a poor REM ‘on switch’ and preponderance in slow and high-voltage sleep, is proposed.

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“…The two main structures directly transmitting sensorimotor information to the dorsal CA1 are the entorhinal cortex and septum. The former processes multisensory information from all sensory cortices (visual, auditory, olfactory, somatosensory), including movement-related sensory feedback (Rio-Bermudez and Blumberg, 2021)and was shown to be activated by spontaneous twitches prior to CA1 (Mohns and Blumberg, 2010; Rio-Bermudez et al, 2020; Valeeva et al, 2019a) while the latter is more likely to be involved in transmitting internal information (Fuhrmann et al, 2015; Wang et al, 2015) as well as unexpected environmental stimuli (Zhang et al, 2018). In addition to these two canonical pathways, one cannot exclude the involvement of a direct connection from the brainstem, given their existence in the adult and their role in promoting sleep as well as motor twitches (Liu et al, 2017; Szőnyi et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion

Dard

Leprince

Denis

et al. 2021

Preprint

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Early electrophysiological brain oscillations recorded in preterm babies and newborn rodents are initially mostly ignited by bottom-up sensorimotor activity and only later can detach from external inputs. This is a hallmark of most developing brain areas including the hippocampus, which in the adult brain, functions in integrating external inputs onto internal dynamics. Such developmental disengagement from external inputs is likely a fundamental step for the proper development of cognitive internal models. Despite its importance, the exact timing and circuit basis for this disengagement remain unknown. To address this issue, we have investigated the daily evolution of CA1 dynamics and underlying circuits during the first and second postnatal week of mouse development using a combination of two-photon calcium imaging of neuronal somata and axons in non-anesthetized pups, viral tracing and chemogenetics. We show that the first postnatal week ends with an abrupt switch in the representation of self-motion in CA1. Indeed, most CA1 pyramidal cells switch from activated to inhibited by self-generated movements at the end of the first postnatal week whereas GABAergic neurons remain positively modulated throughout this period. This rapid switch occurs within two days and is mediated by the rapid anatomical and functional surge of somatic inhibition. The observed dynamics is consistent with a two-population model undergoing strengthening inhibition. Remarkably, a transient silencing of local somatostatin-expressing interneurons both prevents the emergence of the perisomatic GABAergic coverage and the disengagement of CA1 hippocampal dynamics from self-motion. We propose that such activity-dependent emergence of feedback inhibitory circuits critically inaugurates the development of internal cognitive models.

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Sleep as a window on the sensorimotor foundations of the developing hippocampus

Cited by 11 publications

References 121 publications

Activity in developing prefrontal cortex is shaped by sleep and sensory experience

Activity in developing prefrontal cortex is shaped by sleep and sensory experience

Literature Cases Summarized Based on Their Polysomnographic Findings in Rett Syndrome

The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion

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