Early brain activity: Translations between bedside and laboratory

Luhmann, Heiko J.; Molnár, Zoltán; Vanhatalo, Sampsa

doi:10.1016/j.pneurobio.2022.102268

Cited by 17 publications

(19 citation statements)

References 256 publications

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“…In humans, studies on brain functions are not easy to be performed as they can be invasive and unfeasible, particularly so on pregnant women, fetuses, and newborns. On the other hand, human neurodevelopment has unique and specific features that are associated with extraordinary mental capabilities, including cognitive and affective abilities, which distinguish humans from other primates; hence, they cannot be inferred from animal model studies (Bibb et al, 2001;Clancy et al, 2001;Clowry et al, 2010;Judaš et al, 2013;Foster et al, 2020;Luhmann et al, 2022). Herein, human studies have been referred to when available, and animal studies have been considered taking into account all relevant differences.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, in mice, ipRGCs' light response in utero has been considered to be fundamental for the vascular patterning of the retina (Rao et al, 2013). However, to what extent this applies to human fetal eye development still remains to be investigated (Hazelhoff et al, 2021;Luhmann et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…In particular, this pattern disappears around the end of the first postnatal week. Spontaneous and evoked delta-brushes can be observed in the somatosensory cortex of premature human neonates of 28-32 weeks of postconceptional age (Milh et al, 2007;Luhmann et al, 2014Luhmann et al, , 2018Luhmann et al, , 2022Molnár et al, 2020;Shibata and Otsubo, 2020;Kidokoro, 2021). Delta brushes in preterm human infants correlate with the so-called spindle bursts, recorded in rodents during the early postnatal period Colonnese and Khazipov, 2012;Yang et al, 2016).…”

Section: The Newborn's Likelihood To Survive and The Activation Of Sp...mentioning

confidence: 95%

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The Newborn's Reaction to Light as the Determinant of the Brain's Activation at Human Birth

Polese

Riccio

Fagioli

et al. 2022

Front. Integr. Neurosci.

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Developmental neuroscience research has not yet fully unveiled the dynamics involved in human birth. The trigger of the first breath, often assumed to be the marker of human life, has not been characterized nor has the process entailing brain modification and activation at birth been clarified yet. To date, few researchers only have investigated the impact of the extrauterine environment, with its strong stimuli, on birth. This ‘hypothesis and theory' article assumes the role of a specific stimulus activating the central nervous system (CNS) at human birth. This stimulus must have specific features though, such as novelty, efficacy, ubiquity, and immediacy. We propose light as a robust candidate for the CNS activation via the retina. Available data on fetal and neonatal neurodevelopment, in particular with reference to retinal light-responsive pathways, will be examined together with the GABA functional switch, and the subplate disappearance, which, at an experimental level, differentiate the neonatal brain from the fetal brain. In this study, we assume how a very rapid activation of retinal photoreceptors at birth initiates a sudden brain shift from the prenatal pattern of functions to the neonatal setup. Our assumption implies the presence of a photoreceptor capable of capturing and transducing light/photon stimulus, transforming it into an effective signal for the activation of new brain functions at birth. Opsin photoreception or, more specifically, melanopsin-dependent photoreception, which is provided by intrinsically photosensitive retinal ganglion cells (ipRGCs), is considered as a valid candidate. Although what is assumed herein cannot be verified in humans based on knowledge available so far, proposing an important and novel function can trigger a broad range of diversified research in different domains, from neurophysiology to neurology and psychiatry.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: The Newborn's Likelihood To Survive and The Activation Of Sp...mentioning

confidence: 95%

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The Newborn's Reaction to Light as the Determinant of the Brain's Activation at Human Birth

Polese

Riccio

Fagioli

et al. 2022

Front. Integr. Neurosci.

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“…Spontaneous activity in the developing cortex evolves from uncorrelated neuronal firing to synchronized network oscillations in local neuronal assemblies (for review, see Egorov and Draguhn, 2013 ; Molnár et al, 2020 ). Here, synchronous network activity is marked by discontinuous high frequency oscillations, which are observed at regular intervals in several animal models, both in vivo and in vitro ( Allène et al, 2008 ; Yang et al, 2009 ; for review, see Khazipov and Luhmann, 2006 ; Luhmann et al, 2022 ). At the cellular level, these rhythmic discharges translate into bursts of action potentials ( Cunningham et al, 2004 ; Minlebaev et al, 2007 ), which are thought to strengthen synaptic contacts ( Winnubst et al, 2015 ) and ensure communication between neurons (for review, see Lisman, 1997 ).…”

Section: Introductionmentioning

confidence: 99%

Spontaneous Activity Predicts Survival of Developing Cortical Neurons

Warm

Bassetti

Schroer

et al. 2022

Front. Cell Dev. Biol.

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Spontaneous activity plays a crucial role in brain development by coordinating the integration of immature neurons into emerging cortical networks. High levels and complex patterns of spontaneous activity are generally associated with low rates of apoptosis in the cortex. However, whether spontaneous activity patterns directly encode for survival of individual cortical neurons during development remains an open question. Here, we longitudinally investigated spontaneous activity and apoptosis in developing cortical cultures, combining extracellular electrophysiology with calcium imaging. These experiments demonstrated that the early occurrence of calcium transients was strongly linked to neuronal survival. Silent neurons exhibited a higher probability of cell death, whereas high frequency spiking and burst behavior were almost exclusively detected in surviving neurons. In local neuronal clusters, activity of neighboring neurons exerted a pro-survival effect, whereas on the functional level, networks with a high modular topology were associated with lower cell death rates. Using machine learning algorithms, cell fate of individual neurons was predictable through the integration of spontaneous activity features. Our results indicate that high frequency spiking activity constrains apoptosis in single neurons through sustained calcium rises and thereby consolidates networks in which a high modular topology is reached during early development.

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“…It has been demonstrated that transient bursts of neural activity, which characterize the brain during this dynamic period, are critical for many developmental processes including neuronal migration and synaptic refinement (Katz & Shatz, 1996; Heck et al ., 2008; Bonetti & Surace, 2010; Yasuda et al ., 2011; Bando et al ., 2016; Minocha et al ., 2017; Suchkov et al ., 2018; Yasuda et al ., 2021). Disruption of these early patterns of activity can lead to aberrant neuronal circuit development and lasting cognitive impairments in animal models (Hartung et al ., 2016b; Chini & Hanganu-Opatz, 2020; Chini et al ., 2020; Bitzenhofer et al ., 2021) and likely contribute also to the emergence of a variety of neurodevelopmental and neurological disorders including schizophrenia, autism and epilepsy, amongst others (Graybiel & Rauch, 2000; Del Campo et al ., 2011; Langen et al ., 2011; McNaught & Mink, 2011; Shepherd, 2013; Albin, 2018; Chini & Hanganu-Opatz, 2020; Molnar et al ., 2020; Iannone & De Marco Garcia, 2021; Luhmann et al ., 2022). Many studies of these patterns of activity have been performed in cortical structures (Hanganu et al ., 2006; Brockmann et al ., 2011; An et al ., 2014; Cichon et al ., 2014; Shen & Colonnese, 2016) or related afferent structures such as thalamus (Weliky & Katz, 1999; Minlebaev et al ., 2011; Yang et al ., 2013).…”

Section: Introductionmentioning

confidence: 99%

Generation and propagation of network bursts in the basal ganglia exhibit dynamic changes during early postnatal development

Klavinskis-Whiting

Bitzenhofer

Hanganu‐Opatz

et al. 2022

Preprint

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The neonatal brain is characterised by intermittent bursts of oscillatory activity interspersed by relative silence. While these bursts of activity are well characterised for many cortical areas much less is known whether and how these propagate and interact with subcortical regions. Here, early network activity was recorded using silicon probes from the developing basal ganglia, including the motor/somatosensory cortex, dorsal striatum and intralaminar thalamus, during the first two postnatal weeks in mice. Using an unsupervised detection and classification method, two main classes of bursting activity were found, consisting of spindle bursts (SB) and nested gamma spindle bursts (NGB), which were characterised by oscillatory activity at respectively ~10 Hz and ~30 Hz. These bursts were reliably identified across all three brain structures but differed in their structural, spectral, and developmental characteristics. Coherence and cross-correlation analyses revealed that burst events often occur synchronously across different brain regions and were mostly of a similar type, especially between cortex and striatum, which also exhibited the strongest interactions as compared to other brain regions. Interestingly, the preferred frequency for these interactions suggested a developmental shift from initial lower frequencies to higher frequencies across development. Together, these results provide the first detailed description of early network activity within the developing basal ganglia and suggests that distinct brain regions drive and coordinate burst activity at different developmental stages.

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Early brain activity: Translations between bedside and laboratory

Cited by 17 publications

References 256 publications

The Newborn's Reaction to Light as the Determinant of the Brain's Activation at Human Birth

The Newborn's Reaction to Light as the Determinant of the Brain's Activation at Human Birth

Spontaneous Activity Predicts Survival of Developing Cortical Neurons

Generation and propagation of network bursts in the basal ganglia exhibit dynamic changes during early postnatal development

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