Spontaneous activity in developing thalamic and cortical sensory networks

Martini, Francisco J.; Guillamón-Vivancos, Teresa; Moreno‐Juan, Verónica; Valdeolmillos, Miguel; López‐Bendito, Guillermina

doi:10.1016/j.neuron.2021.06.026

Cited by 114 publications

(101 citation statements)

References 203 publications

(249 reference statements)

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“…In general, the importance of distinct cortical activity patterns during cortical development is emphasized by their necessity for and coherent emergence with higher cognitive function (Tort et al, 2009;Bosman et al, 2012). Consistently, in sensory cortical areas during the postnatal period of rodents, stereotypical spontaneous and evoked activity patterns concurrently develop with respective sensory modalities (Rochefort et al, 2009;Yang et al, 2009;Colonnese et al, 2010;Ackman and Crair, 2014;Martini et al, 2021). However, the source of spontaneous activity is still a matter of ongoing research, as well as the root cause and type of evoked activity which varies depending on the region and time point of perinatal development.…”

Section: Introductionmentioning

confidence: 98%

“…Starting with the formation of the first GABAergic synapse (Khazipov et al, 2001 ), the maturation of the inhibitory system coincides with the emergence of correlated oscillatory activity patterns, such as spindle burst and gamma oscillations in newborn rodents or delta brushes in prenatal humans (Luhmann and Khazipov, 2018 ). Here, the thalamus contributes significantly to the generation of these early cortical oscillations (Minlebaev et al, 2011 ; Yang et al, 2013 ; Murata and Colonnese, 2016 ), which conversely also modulate thalamic activity within a cortico-thalamic feedback loop (Yang et al, 2013 ; Martini et al, 2021 ). Furthermore, the maturation of the adult inhibitory GABAergic system is still not complete when cortical activity evolves to its final more de-correlated activity state that underlies its later complex functions (Golshani et al, 2009 ; Rochefort et al, 2009 ).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, it comes to no surprise that neuronal activity also strongly impacts the maturation of the GABAergic system, from the cellular to the network level, and fine-tunes excitation/inhibition balance (Turrigiano and Nelson, 2004 ; Takesian and Hensch, 2013 ). Besides cortical activity, thalamic inputs also play a role in interneuron maturation on the level of the cortex (Pouchelon et al, 2014 ; Marques-Smith et al, 2016 ), while interneurons in turn function as a gate for the thalamus by effecting cortical network activity (Yang et al, 2013 ; Martini et al, 2021 ). Therefore, the GABAergic system must permit sufficient excitation to engage in cortical activity and still provide the needed inhibition to prevent over-excitation.…”

Section: Introductionmentioning

confidence: 99%

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Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity

Warm

Schroer

Sinning

2022

Front. Mol. Neurosci.

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Throughout early phases of brain development, the two main neural signaling mechanisms—excitation and inhibition—are dynamically sculpted in the neocortex to establish primary functions. Despite its relatively late formation and persistent developmental changes, the GABAergic system promotes the ordered shaping of neuronal circuits at the structural and functional levels. Within this frame, interneurons participate first in spontaneous and later in sensory-evoked activity patterns that precede cortical functions of the mature brain. Upon their subcortical generation, interneurons in the embryonic brain must first orderly migrate to and settle in respective target layers before they can actively engage in cortical network activity. During this process, changes at the molecular and synaptic level of interneurons allow not only their coordinated formation but also the pruning of connections as well as excitatory and inhibitory synapses. At the postsynaptic site, the shift of GABAergic signaling from an excitatory towards an inhibitory response is required to enable synchronization within cortical networks. Concomitantly, the progressive specification of different interneuron subtypes endows the neocortex with distinct local cortical circuits and region-specific modulation of neuronal firing. Finally, the apoptotic process further refines neuronal populations by constantly maintaining a controlled ratio of inhibitory and excitatory neurons. Interestingly, many of these fundamental and complex processes are influenced—if not directly controlled—by electrical activity. Interneurons on the subcellular, cellular, and network level are affected by high frequency patterns, such as spindle burst and gamma oscillations in rodents and delta brushes in humans. Conversely, the maturation of interneuron structure and function on each of these scales feeds back and contributes to the generation of cortical activity patterns that are essential for the proper peri- and postnatal development. Overall, a more precise description of the conducting role of interneurons in terms of how they contribute to specific activity patterns—as well as how specific activity patterns impinge on their maturation as orchestra members—will lead to a better understanding of the physiological and pathophysiological development and function of the nervous system.

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Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity

Warm

Schroer

Sinning

2022

Front. Mol. Neurosci.

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“…Over the last decade we got deeper insights into the functional roles of these early cortical activity patterns. During embryonic stages spontaneous activity arising from the thalamus regulates coordinate cortical sensory area patterning and drives the emergence of functional cortical maps (Moreno-Juan et al, 2017 ; Anton-Bolanos et al, 2018 , 2019 ; Martini et al, 2021 ). In newborn rodent cortex spontaneous and sensory evoked cortical activity often locally synchronizes column-like networks resembling early topographic cortical maps (Yang et al, 2013 ; Kummer et al, 2016 ).…”

Section: Neurophysiology Of the Developing Cerebral Cortex: What We Have Learnedmentioning

confidence: 99%

Neurophysiology of the Developing Cerebral Cortex: What We Have Learned and What We Need to Know

Luhmann

2022

Front. Cell. Neurosci.

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This review article aims to give a brief summary on the novel technologies, the challenges, our current understanding, and the open questions in the field of the neurophysiology of the developing cerebral cortex in rodents. In the past, in vitro electrophysiological and calcium imaging studies on single neurons provided important insights into the function of cellular and subcellular mechanism during early postnatal development. In the past decade, neuronal activity in large cortical networks was recorded in pre- and neonatal rodents in vivo by the use of novel high-density multi-electrode arrays and genetically encoded calcium indicators. These studies demonstrated a surprisingly rich repertoire of spontaneous cortical and subcortical activity patterns, which are currently not completely understood in their functional roles in early development and their impact on cortical maturation. Technological progress in targeted genetic manipulations, optogenetics, and chemogenetics now allow the experimental manipulation of specific neuronal cell types to elucidate the function of early (transient) cortical circuits and their role in the generation of spontaneous and sensory evoked cortical activity patterns. Large-scale interactions between different cortical areas and subcortical regions, characterization of developmental shifts from synchronized to desynchronized activity patterns, identification of transient circuits and hub neurons, role of electrical activity in the control of glial cell differentiation and function are future key tasks to gain further insights into the neurophysiology of the developing cerebral cortex.

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“…This finding likely underlies the key role of the thalamus in auditory information transfer. The thalamus, which consists of many nuclei, is the relaying nucleus of the sensory pathway and receives input from the cortex (Hwang et al, 2017;Martini et al, 2021). It also mediates important functions including memory, emotion, and attention (Arend et al, 2015;Geier et al, 2020).…”

Section: Topological Parameter Alterationsmentioning

confidence: 99%

Altered Functional Network in Infants With Profound Bilateral Congenital Sensorineural Hearing Loss: A Graph Theory Analysis

et al. 2022

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Functional magnetic resonance imaging (fMRI) studies have suggested that there is a functional reorganization of brain areas in patients with sensorineural hearing loss (SNHL). Recently, graph theory analysis has brought a new understanding of the functional connectome and topological features in central neural system diseases. However, little is known about the functional network topology changes in SNHL patients, especially in infants. In this study, 34 infants with profound bilateral congenital SNHL and 28 infants with normal hearing aged 11–36 months were recruited. No difference was found in small-world parameters and network efficiency parameters. Differences in global and nodal topologic organization, hub distribution, and whole-brain functional connectivity were explored using graph theory analysis. Both normal-hearing infants and SNHL infants exhibited small-world topology. Furthermore, the SNHL group showed a decreased nodal degree in the bilateral thalamus. Six hubs in the SNHL group and seven hubs in the normal-hearing group were identified. The left middle temporal gyrus was a hub only in the SNHL group, while the right parahippocampal gyrus and bilateral temporal pole were hubs only in the normal-hearing group. Functional connectivity between auditory regions and motor regions, between auditory regions and default-mode-network (DMN) regions, and within DMN regions was found to be decreased in the SNHL group. These results indicate a functional reorganization of brain functional networks as a result of hearing loss. This study provides evidence that functional reorganization occurs in the early stage of life in infants with profound bilateral congenital SNHL from the perspective of complex networks.

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Spontaneous activity in developing thalamic and cortical sensory networks

Cited by 114 publications

References 203 publications

Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity

Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity

Neurophysiology of the Developing Cerebral Cortex: What We Have Learned and What We Need to Know

Altered Functional Network in Infants With Profound Bilateral Congenital Sensorineural Hearing Loss: A Graph Theory Analysis

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