Pathway-specific asymmetries between on and off visual signals
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Abstract
Visual processing is largely organized into ON and OFF pathways that signal stimulus increments and decrements, respectively. These pathways exhibit natural pairings based on morphological and physiological similarities, such as ON and OFF α-ganglion cells in the mammalian retina. Several studies have noted asymmetries in the properties of ON and OFF pathways. For example, the spatial receptive fields (RFs) of OFF α-cells are systematically smaller than ON α-cells. Analysis of natural scenes suggests that these asymmetries are optimal for visual encoding. To test the generality of ON/OFF asymmetries, we measured the spatiotemporal RF properties of multiple RGC types in rat retina. Through a quantitative and serial classification, we identified three functional pairs of ON and OFF RGCs. We analyzed the structure of their RFs and compared spatial integration, temporal integration, and gain across ON and OFF pairs. Similar to previous results from the cat and primate, RGC types with larger spatial RFs exhibited briefer temporal integration and higher gain. However, each pair of ON and OFF RGC types exhibited distinct asymmetric relationships between RF properties, some of which were opposite to the findings of previous reports. These results reveal the functional organization of six RGC types in the rodent retina and indicate that ON/OFF asymmetries are pathway specific. SIGNIFICANCE STATEMENT Circuits that process sensory input frequently process increments separately from decrements, so-called ON and OFF responses. Theoretical studies indicate that this separation, and associated asymmetries in ON and OFF pathways, may be beneficial for encoding natural stimuli. However, the generality of ON and OFF pathway asymmetries has not been tested. Here we compare the functional properties of three distinct pairs of ON and OFF pathways in the rodent retina and show that their asymmetries are pathway specific. These results provide a new view on the partitioning of vision across diverse ON and OFF signaling pathways.
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In the rat retina, putative ON brisk transient and OFF brisk transient cells formed reasonably complete mosaics covering the region recorded and had properties broadly resembling those of ON and OFF parasol cells in the macaque retina.
“In the rat retina, analysis was restricted to two RGC types – putative ON brisk transient and OFF brisk transient cells identified by their receptive fields and spiking autocorrelation (Ravi et al., 2018) – which formed reasonably complete mosaics covering the region recorded and had properties broadly resembling those of ON and OFF parasol cells in the macaque retina.”
From Precise control of neural activity using dynamically optimized electrical stimulation (2024) · cites this paper as Ravi et al., 2018
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Girman, S. V., & Lund, R. D. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00517.2010 · Cited by 14 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Dacey D (2004) Origins of perception: retinal ganglion cell diversity and the creation of parallel visual pathways. In: The cognitive neurosciences (Gaz- zaniga MS, ed), pp 281-301. Cambridge, MA: MIT.
Cited by
Sorted by citations
Precise control of neural activity using dynamically optimized electrical stimulation
Shah, N. P., Phillips, A., Madugula, S., Lotlikar, A., Gogliettino, A. R., Hays, M. R., Grosberg, L., Brown, J., Dusi, A., Tandon, P., et al. (2024) · eLife · doi:10.7554/elife.83424 · Cited by 15 · see citing works
Self-citation
- Authors
- Ravi, S., Ahn, D., Greschner, M., Chichilnisky, E. J., & Field, G. D.
- Affiliations
- Duke University (US)
- Salk Institute for Biological Studies (US)
- Carl von Ossietzky Universität Oldenburg (DE)
- Stanford Medicine (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-09-24
- Volume
- 38
- Issue
- 45
- Pages
- 9728-9740
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6222062
- OpenAlex
- W2952238330
- Cited by
- 63
- References
- 101
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 10 · 2023: 7 · 2022: 14 · 2021: 7 · 2020: 5 · 2019: 6 · 2018: 2 · 2017: 1
- FWCI
- 2.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Whitehall Foundation
- Karl Kirchgessner Foundation
- National Institutes of Health
- National Eye Institute (P30EY019005, R01EY017992, R01EY027193, R01EY024567, R01EY021271)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- ON and OFF pathways, retinal ganglion cells, receptive fields, spatial integration, temporal integration, gain, rodent retina
- MeSH terms
- Action Potentials, Animals, Photic Stimulation, Random Allocation, Retinal Ganglion Cells, Visual Pathways, Rats, Long-Evans, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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