Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity
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 ord...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-01-01
|
| Series: | Frontiers in Molecular Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnmol.2021.807969/full |
| _version_ | 1818732653284687872 |
|---|---|
| author | Davide Warm Jonas Schroer Anne Sinning |
| author_facet | Davide Warm Jonas Schroer Anne Sinning |
| author_sort | Davide Warm |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-17T23:36:59Z |
| format | Article |
| id | doaj.art-689d0fd3396347f4a0461b510ac34387 |
| institution | Directory Open Access Journal |
| issn | 1662-5099 |
| language | English |
| last_indexed | 2024-12-17T23:36:59Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Molecular Neuroscience |
| spelling | doaj.art-689d0fd3396347f4a0461b510ac343872022-12-21T21:28:32ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992022-01-011410.3389/fnmol.2021.807969807969Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network ActivityDavide WarmJonas SchroerAnne SinningThroughout 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.https://www.frontiersin.org/articles/10.3389/fnmol.2021.807969/fullcortexdevelopmentactivity patternsinterneuronGABA shiftapoptosis |
| spellingShingle | Davide Warm Jonas Schroer Anne Sinning Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity Frontiers in Molecular Neuroscience cortex development activity patterns interneuron GABA shift apoptosis |
| title | Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity |
| title_full | Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity |
| title_fullStr | Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity |
| title_full_unstemmed | Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity |
| title_short | Gabaergic Interneurons in Early Brain Development: Conducting and Orchestrated by Cortical Network Activity |
| title_sort | gabaergic interneurons in early brain development conducting and orchestrated by cortical network activity |
| topic | cortex development activity patterns interneuron GABA shift apoptosis |
| url | https://www.frontiersin.org/articles/10.3389/fnmol.2021.807969/full |
| work_keys_str_mv | AT davidewarm gabaergicinterneuronsinearlybraindevelopmentconductingandorchestratedbycorticalnetworkactivity AT jonasschroer gabaergicinterneuronsinearlybraindevelopmentconductingandorchestratedbycorticalnetworkactivity AT annesinning gabaergicinterneuronsinearlybraindevelopmentconductingandorchestratedbycorticalnetworkactivity |