Development of Direction Selectivity in Mouse Cortical Neurons

Rochefort, Nathalie L.; Narushima, Madoka; Grienberger, Christine; Marandi, Nima; Hill, Daniel; Konnerth, Arthur

doi:10.1016/j.neuron.2011.06.013

Cited by 168 publications

(181 citation statements)

References 47 publications

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“…A second difference with the previous MEA study is that alignment of the preferred directions along the temporal and ventral quadrants were overrepresented [5,32], a bias that persisted in recordings from V1 at eye-opening [33] but was not seen here ( Figure 2; Figure S3). Interestingly, it was recently shown that DSGC preferred directions vary retinotopically (Sabbah, S., Gemmer, J., Castro, G., Siegel, J.…”

Section: Distribution Of Dsgc Preferred Directions Along the Cardinalcontrasting

confidence: 82%

Role for Visual Experience in the Development of Direction-Selective Circuits

Bos¹,

Gainer²,

Feller³

2017

Current Biology

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SUMMARYVisually-guided behavior can depend critically on detecting the direction of object movement. This computation is first performed in the retina where direction is encoded by direction-selective ganglion cells (DSGCs) that respond strongly to an object moving in the preferred direction and weakly to an object moving in the opposite, or null, direction (reviewed in [1]). These DSGCs come in multiple types that are classified based on their morphologies, response properties and targets in the brain. This study focuses on two types -ON and ON-OFF DSGCs. Though animals can sense motion in all directions, the preferred directions of DSGCs in adult retina cluster along distinct directions that we refer to as the cardinal axes. ON DSGCs have three cardinal axestemporal, ventral and dorsonasal -while ON-OFF DSGCs have four -nasal, temporal, dorsal, and ventral. How these preferred directions emerge during development is still not understood. Several studies have demonstrated that ON [2] and ON-OFF DSGCs are well tuned at eye-opening, and even a few days prior to eye-opening, in rabbits [3], rats [4] and mice [5][6][7][8], suggesting that visual experience is not required to produce direction selective tuning. However, here we show that at eye-opening the preferred directions of both ON and ON-OFF DSGCs are diffusely distributed and that visual deprivation prevents the preferred directions from clustering along the cardinal axes. Our findings indicate a critical role for visual experience in shaping responses in the retina. HHS Public Access RESULTS Clustering of DSGC preferred directions along cardinal axes after eye-opening requires visual experienceWe used two-photon calcium imaging to study the development of DSGC populations in mouse retina. This imaging technique has proven to be quite powerful in characterizing the receptive field properties of retinal ganglion cells [9][10][11][12]. We loaded retinas of WT mice near eye-opening (P13-P14) and in adulthood (>P30) with the calcium dye Oregon green 488 BAPTA-1 hexapotassium salt (OGB-1) via electroporation, thus uniformly labeling the ganglion cell layer ( Figure 1A; see Supplemental Information). Ventral portions of the retina were stimulated with light centered at 385 nm to maximally activate UV-cones [13,14] while minimizing cross talk with the imaging detectors ( Figure S1). This approach allowed us to record from all DSGC subtypes within a single field of view (~40000 μm 2 ).To identify DSGCs, we first used full field UV-light flashes to classify cells as ON, OFF or ON-OFF retinal ganglion cells (RGCs) ( Figure S1; Table S1). We found that around 80% of the cells in the ganglion cell layer of young and adult retinas responded to light flashes with changes in fluorescence (Table S1), similar to the RGC percentages reported in previous studies [9,11,12]. In addition, over development we observed a decrease in the percentage of ON-OFF RGCs (28.03% at P13-14 to 20.84% in adult) (Table S1) [15].Second, we used light bars on a dark background drifting in 8 dir...

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Section: Distribution Of Dsgc Preferred Directions Along the Cardinalcontrasting

confidence: 82%

Role for Visual Experience in the Development of Direction-Selective Circuits

Bos¹,

Gainer²,

Feller³

2017

Current Biology

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“…No maps for stimulus orientation, direction, ocular dominance, or binocular disparity have been reported in the visual cortex of adult wild-type rodents 6,[19][20][21] . However, the ease of loading neurons with fluorescent dyes and attaining imaging stability, together with the powerful genetic tools available for mice has resulted in the vast majority of studies using two-photon imaging of the cerebral cortex being performed in rodents instead of ferrets, cats, and monkeys.…”

Section: Discussionmentioning

confidence: 99%

Targeted Labeling of Neurons in a Specific Functional Micro-domain of the Neocortex by Combining Intrinsic Signal and Two-photon Imaging

O’Herron

Shen²,

Lu³

et al. 2012

JoVE

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In the primary visual cortex of non-rodent mammals, neurons are clustered according to their preference for stimulus features such as orientation [1][2][3][4] , direction [5][6][7] , ocular dominance 8,9 and binocular disparity 9 . Orientation selectivity is the most widely studied feature and a continuous map with a quasi-periodic layout for preferred orientation is present across the entire primary visual cortex 10,11 . Integrating the synaptic, cellular and network contributions that lead to stimulus selective responses in these functional maps requires the hybridization of imaging techniques that span sub-micron to millimeter spatial scales. With conventional intrinsic signal optical imaging, the overall layout of functional maps across the entire surface of the visual cortex can be determined 12 . The development of in vivo two-photon microscopy using calcium sensitive dyes enables one to determine the synaptic input arriving at individual dendritic spines 13 or record activity simultaneously from hundreds of individual neuronal cell bodies 6,14 . Consequently, combining intrinsic signal imaging with the sub-micron spatial resolution of two-photon microscopy offers the possibility of determining exactly which dendritic segments and cells contribute to the micro-domain of any functional map in the neocortex. Here we demonstrate a high-yield method for rapidly obtaining a cortical orientation map and targeting a specific micro-domain in this functional map for labeling neurons with fluorescent dyes in a non-rodent mammal. With the same microscope used for two-photon imaging, we first generate an orientation map using intrinsic signal optical imaging. Then we show how to target a micro-domain of interest using a micropipette loaded with dye to either label a population of neuronal cell bodies or label a single neuron such that dendrites, spines and axons are visible in vivo. Our refinements over previous methods facilitate an examination of neuronal structure-function relationships with sub-cellular resolution in the framework of neocortical functional architectures. Video LinkThe video component of this article can be found at http://www.jove.com/video/50025/ Protocol 1. Surgical Preparation 1. Induce anesthesia and continuously monitor heart rate, end tidal CO 2 , EEG, and temperature. All procedures were approved by the Institutional Animal Care and Use Committee of the Medical University of South Carolina and were based on those we previously published 9,15 . 2. Expose the dorsal surface of the skull by cutting the skin with a scalpel blade. Dissect the connective tissues overlying the bone using a Brudon curette. Clean the bone using cotton tipped applicators and cotton gauze. Apply bone wax (as needed) to the skull, to stop occasional bleeding through small emissary veins. 3. Attach a titanium or stainless steel head plate to the skull (over the region of interest where the craniotomy will be performed) by using dental cement mixed with black paint (see Materials). A rectangular opening in the ce...

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“…Pattern-motion-selective cells in mouse area V1 could similarly obtain their properties from local V1 component-selective and unclassified directionselective units. Alternatively, they could inherit their direction selectivity from subcortical targets, such as the pathway described by Cruz-Martin et al (2014) originating in direction-selective retinal ganglion cells (Cruz-Martin et al, 2014) and supplying the direction information into the top layers of V1 through the orientation-and direction-selective units found in a mouse LGN shell (Piscopo et al, 2013;Marshel et al, 2011), bypassing layer 4. If the PM-selective cells in mouse V1 inherited their properties from local V1 direction-selective neurons, or LGN directionselective neurons via a process analogous to the monkey MT pooling of V1 inputs as described in cascade models (Rust et al, 2006), one would expect them to show broader direction-tuning bandwidth for gratings compared with component and unclassified cells in V1, strong opponent motion inhibition, and crossangle invariance of PM-selectivity (Rust et al, 2006;Solomon et al, 2011).…”

Section: Origins Of Pattern-motion Selectivity In Mouse V1mentioning

confidence: 99%