Local signal processing in mouse horizontal cell dendrites

Abstract

Most neurons in the central nervous system have elaborate dendritic arbours which come in a large variety of sizes and morphologies (Lefebvre et al., 2015). For many decades, dendrites have been thought to simply relay presynaptic signals to the soma and to the axon terminal system by acting as “passive cables”. However, it has become clear that dendrites are capable of much more than passively integrating synaptic input, they can also act independently and modulate presynaptic signals (reviewed by Branco and Häusser, 2010). Dendritic signal processing has been reported to support sophisticated functions in the cortex, hippocampus, and cerebellum as well as in the retina. In the latter case, multiple processing within one dendrite is essential to process considerable amounts of information from the outside world but, at the same time to use space efficiently: The retina needs to be thin and transparent to reduce light scattering within the tissue. Dendritic processing has already been described in inner retinal neurons (Euler et al., 2002; Grimes et al., 2010; Oesch et al., 2005; Sivyer and Williams, 2013). In the outer retina, the horizontal cell (HC) dendrites, which are directly postsynaptic to the cone photoreceptors (cones) have recently been suggested to be plausible candidates for local signal processing (Grassmeyer and Thoreson, 2017; Jackman et al., 2011; Vroman et al., 2014) despite their involvement in global tasks such as contrast enhancement. To test this hypothesis physiologically, I used two-photon imaging to record calcium (Ca2+) signals in cones and HCs, as well as, cone glutamate release in mouse retinal slices. I used green (578 nm) and ultra violet (UV, 360 nm) light stimuli and recorded from different retinal regions to specifically activate different combinations of medium (M-) and short (S-) wavelength-sensitive opsin expressed in cones. This approach allowed to assess if signals from individual cones remain “isolated” within a local dendritic region of a HC, or if they spread across the entire dendritic tree or, in the electrically coupled HC network. In contrast to what one would expect in a purely globally acting HC (network), responses measured in neighbouring HC compartments varied markedly in their chromatic preference suggesting that HC dendrites are able to process cone input in a highly local manner. Moreover, I found local HC feedback to play a role in shaping the temporal properties of cone output.