Adaptation of spontaneous activity in the developing visual cortex

Wosniack, Marina E.; Kirchner, Jan H.; Chao, Ling Ya; Zabouri, Nawal; Löhmann, Christian; Gjorgjieva, Julijana

doi:10.7554/elife.61619

Cited by 24 publications

(27 citation statements)

References 91 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Additional amplification and modulation is likely provided by transient circuits formed between subplate, thalamus and overlying cortex ( Kanold and Luhmann, 2010 ) and by inhibitory networks within cortex ( Kirmse et al, 2015 ; Murata and Colonnese, 2020 ). Thus, there is significant potential by thalamic and local cortical circuits to modulate firing rates within homeostatically set ranges, possibly by the highly synchronous activities remaining after eye removal ( Wosniack et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Input-Independent Homeostasis of Developing Thalamocortical Activity

Riyahi

Phillips

Colonnese

2021

eNeuro

View full text Add to dashboard Cite

The isocortex of all mammals studied to date shows a progressive increase in the amount and continuity of background activity during early development. In humans the transition from a discontinuous (mostly silent, intermittently bursting) cortex to one that is continuously active is complete soon after birth and is a critical prognostic indicator. In the visual cortex of rodents this switch from discontinuous to continuous background activity occurs during the two days before eye-opening, driven by activity changes in relay thalamus. The factors that regulate the timing of continuity development, which enables mature visual processing, are unknown. Here we test the role of the retina, the primary input, in the development of continuous spontaneous activity in the visual cortex of mice using depth electrode recordings from Enucleated mice in vivo. Bilateral enucleation at postnatal day (P)6, one week prior to the onset of continuous activity, acutely silences cortex, yet firing rates and early oscillations return to normal within two days and show a normal developmental trajectory through P12. Enucleated animals showed differences in silent period duration and continuity on P13 that resolved on P16, and an increase in low frequency power that did not. Our results show that the timing of cortical activity development is not determined by the major driving input to the system. Rather, even during a period of rapid increase in firing rates and continuity, neural activity in the visual cortex is under homeostatic control that is largely robust to the loss of the primary input. SIGNIFICANCE STATEMENTUncovering the mechanistic underpinnings of EEG development is critical to increasing the diagnostic potential of this cheap and portable methodology. An important component of this maturation is the acquisition of activity that is continuous, i.e. lacking silent periods. Here we used background activity in the visual cortex of developing unanesthetized mice to show that the primary sensory input plays little role in the development of continuity and normal firing rates, which instead appear to be regulated by mechanism internal to thalamus and cortex. These findings suggest that damage to driving thalamic inputs will be difficult to detect by EEG, and point to the importance of firing rate homeostasis in regulating even early development.

show abstract

Section: Discussionmentioning

confidence: 99%

Input-Independent Homeostasis of Developing Thalamocortical Activity

Riyahi

Phillips

Colonnese

2021

eNeuro

View full text Add to dashboard Cite

show abstract

“…Therefore, the GABAergic system must permit sufficient excitation to engage in cortical activity and still provide the needed inhibition to prevent over-excitation. In this respect, it is worth mentioning that a certain level of freedom in the excitation/inhibition balance is needed, especially for the establishment of the sensory cortical system during early development (Masquelier et al, 2009 ; Deidda et al, 2015 ; Wosniack et al, 2021 ). Both the GABAergic system and neuronal activity are fulfilling important functions during these critical periods, as discussed in more detail elsewhere (Sale et al, 2010 ; Reha et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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

Warm

Schroer

Sinning

2022

Front. Mol. Neurosci.

View full text Add to dashboard Cite

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.

show abstract

“…In the visual system, spontaneous activity coming from the retina causes synchronized waves with similar spatiotemporal features spreading throughout the superior colliculus and in the primary visual cortex (V1; Ackman et al, 2012 ). In addition, in visual cortex, there are late activity patterns with distinct synchronization features that are not dependent on retinal waves, and might be generated within the cortex itself ( Siegel et al, 2012 ; Gribizis et al, 2019 ; Wosniack et al, 2021 ). In the auditory system, spontaneous activity coming from the cochlea and transmitted by the brainstem activates the inferior colliculus and primary auditory cortex (A1) in highly synchronous patterns ( Babola et al, 2018 ).…”

Section: Spontaneous Activity In the Assembly Of Sensory Circuitsmentioning

confidence: 99%

Epigenetic and Transcriptional Regulation of Spontaneous and Sensory Activity Dependent Programs During Neuronal Circuit Development

Pumo

Kitazawa

Rijli

2022

Front. Neural Circuits

View full text Add to dashboard Cite

Spontaneous activity generated before the onset of sensory transduction has a key role in wiring developing sensory circuits. From axonal targeting, to synapse formation and elimination, to the balanced integration of neurons into developing circuits, this type of activity is implicated in a variety of cellular processes. However, little is known about its molecular mechanisms of action, especially at the level of genome regulation. Conversely, sensory experience-dependent activity implements well-characterized transcriptional and epigenetic chromatin programs that underlie heterogeneous but specific genomic responses that shape both postnatal circuit development and neuroplasticity in the adult. In this review, we focus on our knowledge of the developmental processes regulated by spontaneous activity and the underlying transcriptional mechanisms. We also review novel findings on how chromatin regulates the specificity and developmental induction of the experience-dependent program, and speculate their relevance for our understanding of how spontaneous activity may act at the genomic level to instruct circuit assembly and prepare developing neurons for sensory-dependent connectivity refinement and processing.

show abstract

Adaptation of spontaneous activity in the developing visual cortex

Cited by 24 publications

References 91 publications

Input-Independent Homeostasis of Developing Thalamocortical Activity

Input-Independent Homeostasis of Developing Thalamocortical Activity

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

Epigenetic and Transcriptional Regulation of Spontaneous and Sensory Activity Dependent Programs During Neuronal Circuit Development

Contact Info

Product

Resources

About