Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina

Abstract

Mammalian B-type horizontal cells make contact with both photoreceptor types: the dendrites contact cone photoreceptors, whereas the axon terminal processes contact rods. Despite their distinct synaptic contacts, horizontal cell somata and axon terminals receive a mixture of rod and cone inputs. Interaction of the two photoreceptor systems is essential for adaptation of photoreceptor sensitivity to different levels of background illumination, and horizontal cells play a key role in this adaptation. In this study, we used transgenic mouse lines to examine the contributions of rod and cone photoreceptor inputs to horizontal cell light responses in the mouse retina: rod signals were isolated by recording intracellularly from horizontal cells in a mouse lacking the cone cyclic nucleotide-gated channel, which lacks cone function, and cone signals were assessed using the rhodopsin knock-out mouse, which is a model for pure cone function. We found that both horizontal cell compartments receive a mixture of inputs from both photoreceptor types. To determine whether these inputs arrive via the long axon connecting the compartments or by way of rod-cone gap junctional coupling, we assessed the rod and cone contributions to horizontal cell somatic and axon terminal light responses in the connexin36-deficient mouse retina, which lacks rodcone coupling. Our results confirm that rods and cones are coupled by connexin36, and suggest that signal transmission along the axon is unidirectional: signals are passed from horizontal cell soma to axon terminal but not from axon terminal to soma.

A novel mechanism for switching a neural system from one state to another

“…(A) Visual integration time is shaped, in large part, by a negative feedback loop in the outer retina: photoreceptors send signals forward to both bipolar cells and horizontal cells; the horizontal cells then, in turn, provide negative feedback to the photoreceptors (Baylor et al, 1971; Kleinschmidt and Dowling, 1975; Dowling, 1987). Note that the figure shows only one type of horizontal cell and a generic photoreceptor; this is consistent with our model system, the mouse retina, which has only one type of horizontal cell, and it acts on both rods and cones (Peichl and González-Soriano, 1994; Trumpler et al, 2008; Babai and Thoreson, 2009). ( B , left ) In daylight conditions, horizontal cell feedback is strong.…”

Functional architecture of the retina: Development and disease

“…The ‘axon’ terminal of HI horizontal cells in macaque contact rod photoreceptors, making the HI cells responsive to both rod and cone signals (Verweij et al, 1999). Mouse retina has only one horizontal cell type – the B-type horizontal cell whose dendrites contact cone photoreceptors and axon contacts rod photoreceptors (Peichl and Gonzalez-Soriano, 1994; Trumpler et al, 2008). In contrast to horizontal cells in mice and monkey, zebrafish horizontal cells do not separately connect with rods and cones at distinct cellular compartments (‘axon’ versus ‘dendrite’).…”

Photoreceptor Cell Death Mechanisms in Inherited Retinal Degeneration

“…A correspondingly large number of different animal models for rhodopsin exist, with highly variable onset and progression of the disease [42][43][44]. These rhodopsin mutants, although genetically very heterogeneous, can be roughly categorized into two groups: loss-of-function (as seen for instance in the rhodopsin knock-out) [45,46] or gain-of-function (such as the K296E mutation) [47,48]. Gain-of-function mutations may cause an increased and sometimes constitutive phototransduction activity, leading to low intracellular cGMP levels, while loss-of-function mutations may reduce phototransduction activity and raise cGMP levels [44].…”