Eye opening differentially modulates inhibitory synaptic transmission in the developing visual cortex

Guan, Wuqiang; Cao, Junwei; Liu, Lin-Yun; Zhao, Zhihao; Fu, Yuan Hsing; Yu, Yongchun

doi:10.7554/elife.32337

Cited by 48 publications

(46 citation statements)

References 64 publications

(107 reference statements)

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“…The SST-to-PV weights did not form a specific structure during the developmental phase ( Fig. 2b developmental phase) consistent with experimental literature (Guan et al, 2017).…”

Section: Top-down Signal Triggers Plasticity In the Inhibitory Circuitsupporting

confidence: 90%

Inhibitory microcircuits for top-down plasticity of sensory representations

Wilmes

Clopath

2018

Preprint

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Humans and animals are remarkable at detecting stimuli that predict rewards. While the underlying neural mechanisms are unknown, reward influences plasticity of sensory representations in early sensory areas. The underlying changes in excitatory and inhibitory circuitry are however unclear. Recently, experimental findings suggest that the inhibitory circuits can regulate learning. In addition, the inhibitory neurons in superficial layers are highly modulated by diverse long-range inputs, including reward signals. We, therefore, hypothesise that plasticity of interneuron circuits plays a major role in adjusting stimulus representations. We investigate how top-down modulation by rewards can interact with local excitatory and inhibitory plasticity to induce long-lasting changes in sensory circuitry. Using a computational model of layer 2/3 primary visual cortex, we demonstrate how interneuron networks can store information about the rewarded stimulus to instruct long-term changes in excitatory connectivity in the absence of further reward. In our model, stimulus-tuned somatostatin-positive interneurons (SSTs) develop strong connections to parvalbumin-positive interneurons (PVs) during reward presentation such that they selectively disinhibit the pyramidal layer henceforth. This triggers plasticity in the excitatory neurons, which leads to increased stimulus representation. We make specific testable predictions in terms of the activity of different neuron types. We finally show that this two-stage model allows for translation invariance of the learned representation.

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“…The SST-to-PV weights did not form a specific structure during the developmental phase ( Fig. 2b developmental phase) consistent with experimental literature (Guan et al, 2017).…”

Section: Top-down Signal Triggers Plasticity In the Inhibitory Circuitsupporting

confidence: 90%

Inhibitory microcircuits for top-down plasticity of sensory representations

Wilmes

Clopath

2018

Preprint

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“…This increase co-occurred with the maturation of PV-expressing interneurons (Fig. S2a,b) and the maturation of inhibitory synapses on excitatory neurons 17,18 . Therefore, a developmental transition from SST-dominated to PV-dominated feedback inhibition might underlie the gamma frequency increase across development.…”

Section: Mainmentioning

confidence: 71%

Transient developmental increase of prefrontal activity alters network maturation and causes cognitive dysfunction in adult mice

Bitzenhofer

Pöpplau

Chini

et al. 2019

Preprint

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Disturbed neuronal activity in neuropsychiatric pathologies emerges during development and might cause multifold neuronal dysfunction by interfering with apoptosis, dendritic growth and synapse formation. However, how altered electrical activity early in life impacts neuronal function and behavior of adults is unknown. Here, we address this question by transiently increasing the coordinated activity of layer 2/3 pyramidal neurons in the medial prefrontal cortex of neonatal mice and monitoring long-term functional and behavioral consequences. We show that increased activity during early development causes premature maturation of pyramidal neurons and alters interneuron density. Consequently, reduced inhibitory feedback by fast-spiking interneurons and excitation/inhibition imbalance in prefrontal circuits of young adults result in weaker evoked synchronization in gamma frequency. These structural and functional changes ultimately lead to poorer mnemonic and social abilities. Thus, prefrontal activity during early development actively controls the cognitive performance of adults and might be critical for cognitive symptoms of neuropsychiatric diseases.

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“…Therefore, we speculate that once PV is expressed at P14, PV synapses may be able to keep up even during strong excitation. Indeed, the strength of the synaptic connection between fast spiking interneurons and pyramidal cells in the visual cortex was recently found to increase significantly during eye opening (Guan et al, 2017). More powerful transmission at inhibitory synapses could reduce or prevent the occurrence of H-events, contributing to the progressive desynchronization of spontaneous activity around eye-opening (Rochefort et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Control of spontaneous activity patterns by inhibitory signaling in the developing visual cortex

Leighton

Houwen

Cheyne

et al. 2020

Preprint

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During early development, even before the senses are active, bursts of activity travel across the nervous system. This spontaneously generated activity drives the refinement of synaptic connections, preparing young networks for patterned sensory input. Synaptic fine-tuning relies not only on the presence of spontaneous activity, but also on the specific characteristics of these activity patterns, such as their frequency, amplitude and synchronicity. Here, we provide evidence that these crucial characteristics are shaped by the relative balance of excitation and inhibition, where patterns with distinct characteristics have different excitatory/inhibitory ratios. Inhibition can control whether cells participate during a spontaneous event, as pharmacogenetic suppression of the somatostatin (SST) expressing subtype of inhibitory interneurons increased cell recruitment and lateral spread of events. KeywordsMouse, in vivo, pharmacogenetics, somatostatin expressing interneuron, VIP expressing interneuron, calcium imaging, DREADD

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Eye opening differentially modulates inhibitory synaptic transmission in the developing visual cortex

Cited by 48 publications

References 64 publications

Inhibitory microcircuits for top-down plasticity of sensory representations

Inhibitory microcircuits for top-down plasticity of sensory representations

Transient developmental increase of prefrontal activity alters network maturation and causes cognitive dysfunction in adult mice

Control of spontaneous activity patterns by inhibitory signaling in the developing visual cortex

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