scholarly journals Retinal and callosal activity-dependent chandelier cell elimination shapes binocularity in primary visual cortex

2019 ◽  
Author(s):  
Bor-Shuen Wang ◽  
Maria Sol Bernardez Sarria ◽  
Miao He ◽  
Michael C Crair ◽  
Z. Josh Huang

AbstractIn mammalian primary visual cortex (V1), integration of the left and right visual scene into a binocular percept derives from convergent ipsi- and contralateral geniculocortical inputs and trans-callosal projections between the two hemispheres. However, the underlying developmental mechanisms remain incompletely understood. Using genetic methods in mice we found that during the days before eye-opening, retinal and callosal activity drives massive apoptosis of GABAergic chandelier cells (ChCs) in the binocular region of V1. Blockade of ChC elimination resulted in a contralateral-dominated V1 and deficient binocular vision. As activity patterns within and between retinas prior to vision convey organization of the visual field, their regulation of ChC density through the trans-callosal pathway may prime a nascent binocular territory for subsequent experience-driven tuning during the post-vision critical period.One Sentence SummaryPrior to eye opening the developing retina primes the visual cortex for binocular vision by adjusting the density of a cortical inhibitory neuron type.

Neuron ◽  
2020 ◽  
Author(s):  
Bor-Shuen Wang ◽  
Maria Sol Bernardez Sarria ◽  
Xu An ◽  
Miao He ◽  
Nazia M. Alam ◽  
...  

Author(s):  
Jinwoo Kim ◽  
Min Song ◽  
Se-Bum Paik

AbstractIn the primary visual cortex (V1) of higher mammals, long-range horizontal connections (LHCs) are observed to develop, linking iso-orientation domains of cortical tuning. It is unknown how this feature-specific wiring of circuitry develops before eye opening. Here, we show that LHCs in V1 may originate from spatio-temporally structured feedforward activities generated from spontaneous retinal waves. Using model simulations based on the anatomy and observed activity patterns of the retina, we show that waves propagating in retinal mosaics can initialize the wiring of LHCs by co-activating neurons of similar tuning, whereas equivalent random activities cannot induce such organizations. Simulations showed that emerged LHCs can produce the patterned activities observed in V1, matching topography of the underlying orientation map. We also confirmed that the model can also reproduce orientation-specific microcircuits in salt-and-pepper organizations in rodents. Our results imply that early peripheral activities contribute significantly to cortical development of functional circuits.HighlightsDevelopmental model of long-range horizontal connections (LHCs) in V1 is simulatedSpontaneous retinal waves generate feature-specific wiring of LHCs in visual cortexEmerged LHCs induce orientation-matching patterns of spontaneous cortical activityRetinal waves induce orientation-specific microcircuits of visual cortex in rodentsSignificance statementLong-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, selectively connecting iso-domains of orientation maps. However, it is unknown how such tuning-specific wirings develop before eye-opening. Here, we show that LHCs in V1 originate from the tuning-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings of V1 neurons. Our model also explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is applicable universally to circuits of various mammalian species.


Author(s):  
Bor-Shuen Wang ◽  
Maria Sol Bernardez Sarria ◽  
Miao He ◽  
Michael C. Crair ◽  
Z. Josh Huang

2016 ◽  
Vol 12 (12) ◽  
pp. e1005185 ◽  
Author(s):  
Benjamin R. Cowley ◽  
Matthew A. Smith ◽  
Adam Kohn ◽  
Byron M. Yu

2019 ◽  
Author(s):  
Kyle R. Jenks ◽  
Jason D. Shepherd

ABSTRACTThe normal development of neuronal circuits requires both hard-wired gene expression and experience. Sensory processing, such as vision, is especially sensitive to perturbations in experience. However, the exact contribution of experience to neuronal visual response properties and binocular vision remains unknown. To determine how visual response properties developin vivo, we used single cell resolution two-photon calcium imaging of mouse binocular visual cortex at multiple time-points after eye opening. Few neurons are binocularly responsive immediately after eye opening and respond solely to either the contralateral or ipsilateral eye. Binocular neurons emerge during development, which requires visual experience, and show specific tuning of visual response properties. As binocular neurons emerge, activity between the two eyes becomes more correlated in the neuropil. Since experience-dependent plasticity requires the expression of activity-dependent genes, we determined whether the plasticity geneArcmediates the development of normal visual response properties. Surprisingly, rather than mirroring the effects of visual deprivation, mice that lackArcshow increased numbers of binocular neurons during development. Strikingly, removingArcin adult binocular visual cortex increases the numbers of binocular neurons and recapitulates the developmental phenotype, suggesting cortical circuits that mediate visual processing require ongoing experience-dependent plasticity. Thus, experience is critical for the normal development and maintenance of circuits required to process binocular vision.


2021 ◽  
Author(s):  
Marton Albert Hajnal ◽  
Duy Tran ◽  
Michael Einstein ◽  
Mauricio Vallejo Martelo ◽  
Karen Safaryan ◽  
...  

Primary visual cortex (V1) neurons integrate motor and multisensory information with visual inputs during sensory processing. However, whether V1 neurons also integrate and encode higher-order cognitive variables is less understood. We trained mice to perform a context-dependent cross-modal decision task where the interpretation of identical audio-visual stimuli depends on task context. We performed silicon probe population recordings of neuronal activity in V1 during task performance and showed that task context (whether the animal should base its decision on visual or auditory stimuli) can be decoded during both intertrial intervals and stimulus presentations. Context and visual stimuli were represented in overlapping populations but were orthogonal in the population activity space. Context representation was not static but displayed distinctive dynamics upon stimulus onset and offset. Thus, activity patterns in V1 independently represent visual stimuli and cognitive variables relevant to task execution.


2021 ◽  
Author(s):  
Liming Tan ◽  
Dario L. Ringach ◽  
S. Lawrence Zipursky ◽  
Joshua T. Trachtenberg

Depth perception emerges from the development of binocular neurons in primary visual cortex. Vision is required for these neurons to acquire their mature responses to visual stimuli. A prevalent view is that vision does not influence binocular circuitry until the onset of the critical period, about a week after eye opening, and that this relies on inhibition. Here, we show that vision is required to form binocular neurons and to improve binocular tuning and matching from eye opening until critical period closure. Inhibition is not required for this process, but rather antagonizes it. Vision improves the tuning properties of binocular neurons by strengthening and sharpening ipsilateral eye cortical responses. This progressively changes the population of neurons in the binocular pool and this plasticity is sensitive to interocular differences prior to the critical period. Thus, vision guides binocular plasticity from eye opening and prior to the classically defined critical period.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Marina E Wosniack ◽  
Jan H Kirchner ◽  
Ling-Ya Chao ◽  
Nawal Zabouri ◽  
Christian Lohmann ◽  
...  

Spontaneous activity drives the establishment of appropriate connectivity in different circuits during brain development. In the mouse primary visual cortex, two distinct patterns of spontaneous activity occur before vision onset: local low-synchronicity events originating in the retina and global high-synchronicity events originating in the cortex. We sought to determine the contribution of these activity patterns to jointly organize network connectivity through different activity-dependent plasticity rules. We postulated that local events shape cortical input selectivity and topography, while global events homeostatically regulate connection strength. However, to generate robust selectivity, we found that global events should adapt their amplitude to the history of preceding cortical activation. We confirmed this prediction by analyzing in vivo spontaneous cortical activity. The predicted adaptation leads to the sparsification of spontaneous activity on a slower timescale during development, demonstrating the remarkable capacity of the developing sensory cortex to acquire sensitivity to visual inputs after eye-opening.


2019 ◽  
Author(s):  
Ashley M. Wilson ◽  
Jeffrey M. Beck ◽  
Lindsey L. Glickfeld

AbstractAttentional modulation of neuronal activity in sensory cortex could alter perception by enhancing the local representation of attended stimuli or its behavioral read-out downstream. We tested these hypotheses using a task in which mice are cued on interleaved trials to attend visual or auditory targets. Neurons in primary visual cortex (V1) that encode task stimuli have larger visually-evoked responses when attention is directed toward vision. To determine whether the attention-dependent changes in V1 reflect changes in representation or read-out, we decoded task stimuli and choices from population activity. Surprisingly, both visual and auditory choices can be decoded from V1, but decoding takes advantage of unique activity patterns across modalities. Furthermore, decoding of choices, but not stimuli, is impaired when attention is directed toward the opposite modality. The specific effect on choice suggests behavioral improvements with attention are largely due to targeted read-out of the most informative V1 neurons.


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