Synaptic Basis for Differential Orientation Selectivity between Complex and Simple Cells in Mouse Visual Cortex

SummaryWe study the connectivity principles underlying the emergence of orientation selectivity in primary visual cortex (V1) of mammals lacking an orientation map. We present a computational model in which random connectivity gives rise to orientation selectivity that matches experimental observations. It predicts that mouse V1 neurons should exhibit intricate receptive fields in the two-dimensional frequency domain, causing shift in orientation preferences with spatial frequency. We find evidence for these features in mouse V1 using calcium imaging and intracellular whole cell recordings.

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Metabotropic glutamate receptor type 5 is involved in the formation and modification of orientation selectivity in the mouse visual cortex

Neuroscience Research ◽

10.1016/j.neures.2009.09.1204 ◽

2009 ◽

Vol 65 ◽

pp. S216-S217

Author(s):

Takamasa Yoshida ◽

Toshiki Tani ◽

Masataka Fujita ◽

Mizuho Iwama ◽

Shigeyoshi Itohara ◽

...

Keyword(s):

Visual Cortex ◽

Glutamate Receptor ◽

Metabotropic Glutamate Receptor ◽

Orientation Selectivity ◽

Receptor Type ◽

Metabotropic Glutamate ◽

Mouse Visual Cortex

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Broadening of Inhibitory Tuning Underlies Contrast-Dependent Sharpening of Orientation Selectivity in Mouse Visual Cortex

Journal of Neuroscience ◽

10.1523/jneurosci.3221-12.2012 ◽

2012 ◽

Vol 32 (46) ◽

pp. 16466-16477 ◽

Cited By ~ 37

Author(s):

Y.-t. Li ◽

W.-p. Ma ◽

L.-y. Li ◽

L. A. Ibrahim ◽

S.-z. Wang ◽

...

Keyword(s):

Visual Cortex ◽

Orientation Selectivity ◽

Mouse Visual Cortex

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Orientation tuning depends on spatial frequency in mouse visual cortex

10.1101/069997 ◽

2016 ◽

Cited By ~ 1

Author(s):

Inbal Ayzenshtat ◽

Jesse Jackson ◽

Rafael Yuste

Keyword(s):

Visual Cortex ◽

Spatial Frequency ◽

Visual System ◽

Primary Visual Cortex ◽

Receptive Fields ◽

Orientation Selectivity ◽

Natural Scenes ◽

Response Properties ◽

Layer 2 ◽

Mouse Visual Cortex

AbstractThe response properties of neurons to sensory stimuli have been used to identify their receptive fields and functionally map sensory systems. In primary visual cortex, most neurons are selective to a particular orientation and spatial frequency of the visual stimulus. Using two-photon calcium imaging of neuronal populations from the primary visual cortex of mice, we have characterized the response properties of neurons to various orientations and spatial frequencies. Surprisingly, we found that the orientation selectivity of neurons actually depends on the spatial frequency of the stimulus. This dependence can be easily explained if one assumed spatially asymmetric Gabor-type receptive fields. We propose that receptive fields of neurons in layer 2/3 of visual cortex are indeed spatially asymmetric, and that this asymmetry could be used effectively by the visual system to encode natural scenes.Significance StatementIn this manuscript we demonstrate that the orientation selectivity of neurons in primary visual cortex of mouse is highly dependent on the stimulus SF. This dependence is realized quantitatively in a decrease in the selectivity strength of cells in non-optimum SF, and more importantly, it is also evident qualitatively in a shift in the preferred orientation of cells in non-optimum SF. We show that a receptive-field model of a 2D asymmetric Gabor, rather than a symmetric one, can explain this surprising observation. Therefore, we propose that the receptive fields of neurons in layer 2/3 of mouse visual cortex are spatially asymmetric and this asymmetry could be used effectively by the visual system to encode natural scenes.Highlights–Orientation selectivity is dependent on spatial frequency.–Asymmetric Gabor model can explain this dependence.

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In vivo two-photon imaging analysis of development of direction and orientation selectivity in the mouse visual cortex

Neuroscience Research ◽

10.1016/j.neures.2011.07.1122 ◽

2011 ◽

Vol 71 ◽

pp. e257

Author(s):

Madoka Narushima ◽

Nathalie L. Rochefort ◽

Christine Grienberger ◽

Nima Marandi ◽

Arthur Konnerth

Keyword(s):

Visual Cortex ◽

Orientation Selectivity ◽

Imaging Analysis ◽

Two Photon ◽

Photon Imaging ◽

Two Photon Imaging ◽

Mouse Visual Cortex

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Developmental dynamics of cross-modality in mouse visual cortex

10.1101/150847 ◽

2017 ◽

Cited By ~ 1

Author(s):

Ryoma Hattori ◽

Takao K Hensch

Keyword(s):

Visual Cortex ◽

Orientation Selectivity ◽

Functional Roles ◽

V1 Neurons ◽

Auditory Responses ◽

Functional Maturation ◽

Dark Exposure ◽

Genetic Deletion ◽

Mouse Visual Cortex ◽

Developmental Dynamics

SUMMARYMaturation of GABAergic circuits in primary visual cortex (V1) opens a critical period (CP), a developmental window of enhanced plasticity for visual functions. However, how inhibition promotes the plasticity remains unclear. Here, we investigated the developmental dynamics of auditory responses and audiovisual interactions in mouse V1. Modulation of V1 spiking activity by a transient sound was temporally dynamic with alternating enhancement and suppression phases. When paired with grating visual stimuli, sound-driven spike enhancement and suppression were weaker and stronger with preferred orientation than with non-preferred orientations, respectively, leading to impaired net orientation selectivity in V1 neurons. Strikingly, the net orientation selectivity was impervious to sound specifically during the CP due to equal total amounts of sound-driven spike enhancements and suppressions. This balance of spike modulations at the CP was achieved by the preferential maturation of sound-driven spike suppression. However, further maturation of sound-driven spike enhancement broke the balance after the CP. Spectral analysis of field potentials revealed the enhancement of a GABA-mediated sound-driven power suppression specifically at CP. Reduction of inhibition by 10-day dark-exposure or genetic deletion of GAD65 gene dampened sound-driven spike suppression in V1. Furthermore, acute suppression of either parvalbumin-expressing (PV) or somatostatinexpressing (SST) neurons suggested their early or late recruitments by sound, respectively. Our results point to the dampened net non-visual sensory influence as one of the functional roles of GABA circuit maturation during a developmental CP. The insensitivity of visual selectivity to sound during the CP may promote functional maturation of V1 as visual cortex.

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Emergent Orientation Selectivity from Random Networks in Mouse Visual Cortex

Cell Reports ◽

10.1016/j.celrep.2018.07.054 ◽

2018 ◽

Vol 24 (8) ◽

pp. 2042-2050.e6 ◽

Cited By ~ 11

Author(s):

Jagruti J. Pattadkal ◽

German Mato ◽

Carl van Vreeswijk ◽

Nicholas J. Priebe ◽

David Hansel

Keyword(s):

Visual Cortex ◽

Orientation Selectivity ◽

Random Networks ◽

Mouse Visual Cortex

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Haphazard Wiring of Simple Receptive Fields and Orientation Columns in Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.01202.2003 ◽

2004 ◽

Vol 92 (1) ◽

pp. 468-476 ◽

Cited By ~ 65

Author(s):

Dario L. Ringach

Keyword(s):

Visual Cortex ◽

Ganglion Cell ◽

Retinal Ganglion Cell ◽

Receptive Fields ◽

Orientation Selectivity ◽

Recent Analysis ◽

Retinal Ganglion ◽

Simple Cells ◽

Orientation Map ◽

Orientation Columns

The receptive fields of simple cells in visual cortex are composed of elongated on and off subregions. This spatial arrangement is widely thought to be responsible for the generation of orientation selectivity. Neurons with similar orientation preferences cluster in “columns” that tile the cortical surface and form a map of orientation selectivity. It has been proposed that simple cell receptive fields are constructed by the selective pooling of geniculate receptive fields aligned in space. A recent analysis of monosynaptic connections between geniculate and cortical neurons appears to reveal the existence of “wiring rules” that are in accordance with the classical model. The precise origin of the orientation map is unknown, but both genetic and activity-dependent processes are thought to contribute. Here, we put forward the hypothesis that statistical sampling from the retinal ganglion cell mosaic may contribute to the generation of simple cells and provide a blueprint for orientation columns. Results from computer simulations show that the “haphazard wiring” model is consistent with data on the probability of monosynaptic connections and generates orientation columns and maps resembling those found in the cortex. The haphazard wiring hypothesis could be tested by measuring the correlation between the orientation map and the structure of the retinal ganglion cell mosaic of the contralateral eye.

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Receptive Fields and Response Properties of Neurons in Layer 4 of Ferret Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.00749.2002 ◽

2003 ◽

Vol 89 (2) ◽

pp. 1003-1015 ◽

Cited By ~ 43

Author(s):

W. Martin Usrey ◽

Michael P. Sceniak ◽

Barbara Chapman

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Receptive Fields ◽

Field Structure ◽

Orientation Selectivity ◽

Stimulus Orientation ◽

Orientation Tuning ◽

Simple Cells ◽

Response Properties ◽

Layer 4

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated,on and off subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 ± 1.2° (mean ± SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.

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