Experience shapes chandelier cell function and structure in the visual cortex

Abstract

Detailed characterization of interneuron subtypes in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosynaptic input from local layer 5 pyramidal cells and higher-order cortical regions. Two-photon calcium imaging and convolutional neural network modelling revealed that ChCs are visually responsive but weakly selective for stimulus content. In mice running in a virtual tunnel, ChCs respond strongly to locomotion and halting visual flow, suggesting arousal-related activity. Visuomotor experience in the tunnel diminished visual responses of ChCs and induced structural plasticity of ChC boutons and axon initial segment length. Finally, ChCs only weakly inhibited pyramidal cells. These findings suggest that ChCs provide an arousal-related signal to layer 2/3 pyramidal cells that may modulate their activity and/or gate plasticity of their axon initial segments during behaviorally relevant events.

Axo-axonic synaptic input drives homeostatic plasticity by tuning the axon initial segment structurally and functionally

“…Interneurons can actively control the synaptic plasticity of cortical PNs (58)(59)(60). Plasticity of local inhibitory circuits is critical to excitatory neurons during experience-dependent plasticity and learning (20,(61)(62)(63)(64)(65). Subtype-specific alterations is believed to be able to control synaptic plasticity at subcellular resolution (61).…”

“…Neurons have the ability to tune themselves to maintain the stability of the network at multiple levels (17). Recent studies have shown that AIS undergoes plastic changes in response to alterations in network activity (11,12,(18)(19)(20). The length of the AIS and its precise location relative to the cell body dynamically adapt to global depolarization in cultured dentate granule cells (11).…”

“…Conversely, increased network activity through sensory input or exposure to an enriched environment induces the shortening of the AIS and shapes the channel distribution and neuronal intrinsic excitability (19)(20)(21). Such homeostatic adaptations of AIS at the structural and functional levels are believed to contribute to regulation of neuronal output (22), counteracting pathological conditions under injury or disease, thereby maintaining the stability of dynamic network activity (23).…”

Experience-dependent predictions of feedforward and contextual information in mouse visual cortex

“…Taken together, our results show that activity driven by non-occluded and occluded images occurs in separate populations of L2/3 PyCs. These populations are reminiscent of positive and negative prediction error neurons theorized to exist in L2/3 in the framework of predictive coding 19,28,29 .…”

Axo-axonic synaptic input drives homeostatic plasticity by tuning the axon initial segment structurally and functionally

“…Neurons have the ability to tune themselves to maintain the stability of the network at multiple levels ( 17 ). Recent studies have shown that AIS undergoes plastic changes in response to alterations in network activity ( 11 , 12 , 18 – 20 ). The length of the AIS and its precise location relative to the cell body dynamically adapt to global depolarization in cultured dentate granule cells ( 11 ).…”