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The Synaptic and Morphological Basis of Orientation Selectivity in a Polyaxonal Amacrine Cell of the Rabbit Retina.
- Source :
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The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2015 Sep 30; Vol. 35 (39), pp. 13336-50. - Publication Year :
- 2015
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Abstract
- Much of the computational power of the retina derives from the activity of amacrine cells, a large and diverse group of GABAergic and glycinergic inhibitory interneurons. Here, we identify an ON-type orientation-selective, wide-field, polyaxonal amacrine cell (PAC) in the rabbit retina and demonstrate how its orientation selectivity arises from the structure of the dendritic arbor and the pattern of excitatory and inhibitory inputs. Excitation from ON bipolar cells and inhibition arising from the OFF pathway converge to generate a quasi-linear integration of visual signals in the receptive field center. This serves to suppress responses to high spatial frequencies, thereby improving sensitivity to larger objects and enhancing orientation selectivity. Inhibition also regulates the magnitude and time course of excitatory inputs to this PAC through serial inhibitory connections onto the presynaptic terminals of ON bipolar cells. This presynaptic inhibition is driven by graded potentials within local microcircuits, similar in extent to the size of single bipolar cell receptive fields. Additional presynaptic inhibition is generated by spiking amacrine cells on a larger spatial scale covering several hundred microns. The orientation selectivity of this PAC may be a substrate for the inhibition that mediates orientation selectivity in some types of ganglion cells. Significance statement: The retina comprises numerous excitatory and inhibitory circuits that encode specific features in the visual scene, such as orientation, contrast, or motion. Here, we identify a wide-field inhibitory neuron that responds to visual stimuli of a particular orientation, a feature selectivity that is primarily due to the elongated shape of the dendritic arbor. Integration of convergent excitatory and inhibitory inputs from the ON and OFF visual pathways suppress responses to small objects and fine textures, thus enhancing selectivity for larger objects. Feedback inhibition regulates the strength and speed of excitation on both local and wide-field spatial scales. This study demonstrates how different synaptic inputs are regulated to tune a neuron to respond to specific features in the visual scene.<br /> (Copyright © 2015 the authors 0270-6474/15/3513336-15$15.00/0.)
- Subjects :
- Amacrine Cells drug effects
Animals
Axons drug effects
Dendrites drug effects
Dendrites physiology
Evoked Potentials, Visual drug effects
Evoked Potentials, Visual physiology
GABA Agents pharmacology
Nerve Net drug effects
Nerve Net physiology
Orientation drug effects
Patch-Clamp Techniques
Photic Stimulation
Presynaptic Terminals drug effects
Presynaptic Terminals physiology
Rabbits
Receptors, GABA drug effects
Retina drug effects
Retinal Bipolar Cells drug effects
Retinal Bipolar Cells physiology
Retinal Ganglion Cells drug effects
Retinal Ganglion Cells physiology
Synapses drug effects
Visual Fields drug effects
Visual Fields physiology
Amacrine Cells physiology
Axons physiology
Orientation physiology
Retina physiology
Synapses physiology
Subjects
Details
- Language :
- English
- ISSN :
- 1529-2401
- Volume :
- 35
- Issue :
- 39
- Database :
- MEDLINE
- Journal :
- The Journal of neuroscience : the official journal of the Society for Neuroscience
- Publication Type :
- Academic Journal
- Accession number :
- 26424882
- Full Text :
- https://doi.org/10.1523/JNEUROSCI.1712-15.2015