Synchronous inhibitory pathways create both efficiency and diversity in the retina
Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The v...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 4; pp. 1 - 9 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
25.01.2022
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.2116589119 |
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| Abstract | Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission. |
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| AbstractList | Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission. Complex connections in neural circuits make it difficult to quantitatively assign even the most basic neural computations to the actions of specific neurons. Retinal ganglion cells are most sensitive to changes in intensity across space and over time. This property, caused by a region known as the receptive field surround, improves information transmission about natural scenes. We dynamically manipulated individual interneurons to directly measure their effect on retinal receptive fields, finding that two inhibitory neuron types, horizontal cells and amacrine cells, synchronously create the same contribution to the receptive field surround at different spatial scales. By analyzing large populations of ganglion cells, we show that this arrangement increases diversity in retinal signaling while preserving maximal information transmission about natural scenes. Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission. Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission.Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission. Complex connections in neural circuits make it difficult to quantitatively assign even the most basic neural computations to the actions of specific neurons. Retinal ganglion cells are most sensitive to changes in intensity across space and over time. This property, caused by a region known as the receptive field surround, improves information transmission about natural scenes. We dynamically manipulated individual interneurons to directly measure their effect on retinal receptive fields, finding that two inhibitory neuron types, horizontal cells and amacrine cells, synchronously create the same contribution to the receptive field surround at different spatial scales. By analyzing large populations of ganglion cells, we show that this arrangement increases diversity in retinal signaling while preserving maximal information transmission about natural scenes. Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission. SignificanceComplex connections in neural circuits make it difficult to quantitatively assign even the most basic neural computations to the actions of specific neurons. Retinal ganglion cells are most sensitive to changes in intensity across space and over time. This property, caused by a region known as the receptive field surround, improves information transmission about natural scenes. We dynamically manipulated individual interneurons to directly measure their effect on retinal receptive fields, finding that two inhibitory neuron types, horizontal cells and amacrine cells, synchronously create the same contribution to the receptive field surround at different spatial scales. By analyzing large populations of ganglion cells, we show that this arrangement increases diversity in retinal signaling while preserving maximal information transmission about natural scenes. Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across space and time using a peripheral region known as the surround, a property that improves information transmission about natural scenes. The visual features that construct this fundamental property have not been quantitatively assigned to specific interneurons. Here, we describe a generalizable approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. By directly controlling the gain of individual interneurons in the circuit, we show that rather than transmitting different temporal features, inhibitory horizontal cells and linear amacrine cells synchronously create the linear surround at different spatial scales and that these two components fully account for the surround. By analyzing a large population of ganglion cells, we observe substantial diversity in the relative contribution of amacrine and horizontal cell visual features while still allowing individual cells to increase information transmission under the statistics of natural scenes. Established theories of efficient coding have shown that optimal information transmission under natural scenes allows a diverse set of receptive fields. Our results give a mechanism for this theory, showing how distinct neural pathways synthesize a sensory computation and how this architecture both generates computational diversity and achieves the objective of high information transmission. Description |
| ArticleNumber | e2116589119 |
| Author | Baccus, Stephen A. Naecker, Benjamin N. McIntosh, Lane T. Kastner, David B. Manu, Mihai |
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| Keywords | computational model efficient coding neural circuit receptive field perturbation |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 1Present address: Department of Neurosurgery, Cologne-Merheim Medical Center, Witten/Herdecke University School of Medicine, D-51109 Cologne, Germany. 3Present address: Department of Psychiatry, University of California, San Francisco, CA 94143. Edited by Terrence Sejnowski, Computational Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, CA; received September 8, 2021; accepted December 2, 2021 Author contributions: M.M., L.T.M., and S.A.B. designed research; M.M., D.B.K., and B.N.N. performed research; M.M., L.T.M., D.B.K., and B.N.N. analyzed data; and M.M., L.T.M., D.B.K., and S.A.B. wrote the paper. 2M.M. and L.T.M. contributed equally to this work. |
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| Snippet | Sensory receptive fields combine features that originate in different neural pathways. Retinal ganglion cell receptive fields compute intensity changes across... SignificanceComplex connections in neural circuits make it difficult to quantitatively assign even the most basic neural computations to the actions of... Complex connections in neural circuits make it difficult to quantitatively assign even the most basic neural computations to the actions of specific neurons.... |
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| SubjectTerms | Algorithms Amacrine cells Amacrine Cells - metabolism Biological Sciences Circuits Horizontal cells Information processing Interneurons Interneurons - metabolism Models, Biological Neural coding Neuroscience Retina Retina - physiology Retinal ganglion cells Retinal Ganglion Cells - metabolism Retinal Horizontal Cells - metabolism Synaptic Transmission Temporal variations Visual Pathways |
| Title | Synchronous inhibitory pathways create both efficiency and diversity in the retina |
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