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Outer retinal inhibition – An unexpected guest brings a surprising synthesis

Date/Time: Monday 29 April 2013, 03:00pm - 04:30pm

Speaker: Prof. Maarten Kamermans, Netherlands Institute for Neuroscience (NIN) of the Royal Netherlands Academy of Arts and Scien

Event Location: Life Science Building R103, York University [Location Map]

Abstract Neuronal computations strongly depend on inhibitory interactions. The timing of these inhibitory interactions is crucial for their computational effect. One example of such an inhibitory interaction occurs at the first retinal synapse, where horizontal cells (HC) inhibit photoreceptors. This interaction generates the centre/surround organization of bipolar cell (BC) receptive fields and is crucial for contrast enhancement1,2 and possibly colour constancy3. There are two competing hypotheses for the underlying mechanism: an ephaptic mechanism1,4 and a proton-mediated mechanism5.
Here we show that HCs feed back to photoreceptors via an unexpected synthesis of both mechanisms; a very fast ephaptic mechanism with no synaptic delay and a relatively slow mechanism with a time constant of about 160 ms. The first component is one of the fastest inhibitory processes known. The second component is a fully novel form of synaptic modulation, with a highly unexpected molecular basis. We anticipate that this novel form of synaptic modulation is a general phenomenon occurring also at synapses outside the retina.
These two feedback pathways together form a very efficient computational unit. To reduce spatial redundancies in the visual scene, the mean activity of all cones within the large receptive field of HCs is subtracted from the output of individual cones. If this process was not extremely fast, the surround of BC receptive fields would lag behind the centre when responding to moving stimuli. Conversely, reducing temporal redundancies requires a slow mechanism, so lasting activity can be subtracted from the cone output. The slow component of feedback, we described here, is especially suitable for this role.

1. L. J. Klaassen, et al., "Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels," PLoS. Biol. 9(7), e1001107 (2011).
2. L. M. Chalupa and J. S. Werner, the visual neurosciences (A Bradford Book, The MIT Press, Cambridge, Massachusetts; London, England, 2003).
3. M. Kamermans, D. A. Kraaij, and H. Spekreijse, "The cone/horizontal cell network: a possible site for color constancy," Vis. Neurosci. 15(5), 787 (1998).
4. M. Kamermans, et al., "Hemichannel-mediated inhibition in the outer retina," Science. 292, 1178 (2001).
5. H. Hirasawa and A. Kaneko, "pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels," J. Gen. Physiol. 122(6), 657 (2003).

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