scholarly journals Spontaneous retinal waves generate long-range horizontal connectivity in visual cortex

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.

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.


2017 ◽  
Author(s):  
Mean-Hwan Kim ◽  
Petr Znamenskiy ◽  
Maria Florencia Iacaruso ◽  
Thomas D. Mrsic-Flogel

The rules by which neurons in neocortex choose their synaptic partners are not fully understood. In sensory cortex, intermingled neurons encode different attributes of sensory inputs and relay them to different long-range targets. While neurons with similar responses to sensory stimuli make connections preferentially, the relationship between synaptic connectivity within an area and long-range projection target remains unclear. We examined the local connectivity and visual responses of primary visual cortex neurons projecting to anterolateral (AL) and posteromedial (PM) higher visual areas in mice. Although the response properties of layer 2/3 neurons projecting to different targets were often similar, they avoided making connections with each other. Thus, projection target acts independently of response similarity to constrain local synaptic connectivity of cortical neurons. We propose that this segregated connectivity rule reduces the crosstalk between different populations of projection neurons, allowing top-down signal to modulate the activity of these output channels independently.


Author(s):  
Dimitri Ryczko ◽  
Maroua Hanini-Daoud ◽  
Steven Condamine ◽  
Benjamin J. B. Bréant ◽  
Maxime Fougère ◽  
...  

AbstractThe most complex cerebral functions are performed by the cortex which most important output is carried out by its layer 5 pyramidal neurons. Their firing reflects integration of sensory and contextual information that they receive. There is evidence that astrocytes influence cortical neurons firing through the release of gliotransmitters such as ATP, glutamate or GABA. These effects were described at the network and at the synaptic levels, but it is still unclear how astrocytes influence neurons input-output transfer function at the cellular level. Here, we used optogenetic tools coupled with electrophysiological, imaging and anatomical approaches to test whether and how astrocytic activation affected processing and integration of distal inputs to layer 5 pyramidal neurons (L5PN). We show that optogenetic activation of astrocytes near L5PN cell body prolonged firing induced by distal inputs to L5PN and potentiated their ability to trigger spikes. The observed astrocytic effects on L5PN firing involved glutamatergic transmission to some extent but relied on release of S100β, an astrocytic Ca2+-binding protein that decreases extracellular Ca2+ once released. This astrocyte-evoked decrease of extracellular Ca2+ elicited firing mediated by activation of Nav1.6 channels. Our findings suggest that astrocytes contribute to the cortical fundamental computational operations by controlling the extracellular ionic environment.Key Points SummaryIntegration of inputs along the dendritic tree of layer 5 pyramidal neurons is an essential operation as these cells represent the most important output carrier of the cerebral cortex. However, the contribution of astrocytes, a type of glial cell to these operations is poorly documented.Here we found that optogenetic activation of astrocytes in the vicinity of layer 5 in the mouse primary visual cortex induce spiking in local pyramidal neurons through Nav1.6 ion channels and prolongs the responses elicited in these neurons by stimulation of their distal inputs in cortical layer 1.This effect partially involved glutamatergic signalling but relied mostly on the astrocytic calcium-binding protein S100β, which regulates the concentration of calcium in the extracellular space around neurons.These findings show that astrocytes contribute to the fundamental computational operations of the cortex by acting on the ionic environment of neurons.


2020 ◽  
Vol 40 (34) ◽  
pp. 6584-6599 ◽  
Author(s):  
Jinwoo Kim ◽  
Min Song ◽  
Jaeson Jang ◽  
Se-Bum Paik

2008 ◽  
Vol 100 (3) ◽  
pp. 1476-1487 ◽  
Author(s):  
Bin Zhang ◽  
Earl L. Smith ◽  
Yuzo M. Chino

Vision of newborn infants is limited by immaturities in their visual brain. In adult primates, the transient onset discharges of visual cortical neurons are thought to be intimately involved with capturing the rapid succession of brief images in visual scenes. Here we sought to determine the responsiveness and quality of transient responses in individual neurons of the primary visual cortex (V1) and visual area 2 (V2) of infant monkeys. We show that the transient component of neuronal firing to 640-ms stationary gratings was as robust and as reliable as in adults only 2 wk after birth, whereas the sustained component was more sluggish in infants than in adults. Thus the cortical circuitry supporting onset transient responses is functionally mature near birth, and our findings predict that neonates, known for their “impoverished vision,” are capable of initiating relatively mature fixating eye movements and of performing in detection of simple objects far better than traditionally thought.


2000 ◽  
Vol 84 (4) ◽  
pp. 2048-2062 ◽  
Author(s):  
Mitesh K. Kapadia ◽  
Gerald Westheimer ◽  
Charles D. Gilbert

To examine the role of primary visual cortex in visuospatial integration, we studied the spatial arrangement of contextual interactions in the response properties of neurons in primary visual cortex of alert monkeys and in human perception. We found a spatial segregation of opposing contextual interactions. At the level of cortical neurons, excitatory interactions were located along the ends of receptive fields, while inhibitory interactions were strongest along the orthogonal axis. Parallel psychophysical studies in human observers showed opposing contextual interactions surrounding a target line with a similar spatial distribution. The results suggest that V1 neurons can participate in multiple perceptual processes via spatially segregated and functionally distinct components of their receptive fields.


2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey

The activity of neurons in primary visual cortex is influenced by the orientation, contrast, and temporal frequency of a visual stimulus. This raises the question of how these stimulus properties interact to shape neuronal responses. While past studies have shown that the bandwidth of orientation tuning is invariant to stimulus contrast, the influence of temporal frequency on orientation-tuning bandwidth is unknown. Here, we investigate the influence of temporal frequency on orientation tuning and direction selectivity in area 17 of ferret visual cortex. For both simple cells and complex cells, measures of orientation-tuning bandwidth (half-width at half-maximum response) are ∼20–25° across a wide range of temporal frequencies. Thus cortical neurons display temporal-frequency invariant orientation tuning. In contrast, direction selectivity is typically reduced, and occasionally reverses, at nonpreferred temporal frequencies. These results show that the mechanisms contributing to the generation of orientation tuning and direction selectivity are differentially affected by the temporal frequency of a visual stimulus and support the notion that stability of orientation tuning is an important aspect of visual processing.


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