Feedback from Horizontal Cells to Rod Photoreceptors in Vertebrate Retina

Abstract

Retinal horizontal cells (HCs) provide negative feedback to cones, but, largely because annular illumination fails to evoke a depolarizing response in rods, it is widely believed that there is no feedback from HCs to rods. However, feedback from HCs to cones involves small changes in the calcium current (I Ca ) that do not always generate detectable depolarizing responses. We therefore recorded I Ca directly from rods to test whether they were modulated by feedback from HCs. To circumvent problems presented by overlapping receptive fields of HCs and rods, we manipulated the membrane potential of voltage-clamped HCs while simultaneously recording from rods in a salamander retinal slice preparation. Like HC feedback in cones, hyperpolarizing HCs from Ϫ14 to Ϫ54, Ϫ84, and Ϫ104 mV increased the amplitude of I Ca recorded from synaptically connected rods and caused hyperpolarizing shifts in I Ca voltage dependence. These effects were blocked by supplementing the bicarbonate-buffered saline solution with HEPES. In rods lacking light-responsive outer segments, hyperpolarizing neighboring HCs with light caused a negative activation shift and increased the amplitude of I Ca . These changes in I Ca were blocked by HEPES and by inhibiting HC light responses with a glutamate antagonist, indicating that they were caused by HC feedback. These results show that rods, like cones, receive negative feedback from HCs that regulates the amplitude and voltage dependence of I Ca . HC-to-rod feedback counters light-evoked decreases in synaptic output and thus shapes the transmission of rod responses to downstream visual neurons.

Speeding rod recovery improves temporal resolution in the retina

“…In addition to rod bipolar cells, rods form invaginating synapses with horizontal cells, which play a critical role in establishing surround inhibition (Wassle, 2004), and shape the responses of both rods and cones (Thoreson et al, 2008; Trumpler et al, 2008). Similar to what had been observed in both sets of bipolar recordings, horizontal flicker responses fell in magnitude at higher frequencies, which became more pronounced at brighter intensities (Figure 5).…”

Neuropeptide Y system in the retina: From localization to function

“…Conversely, in the lateral flow, in the OPL and IPL, respectively, horizontal and amacrine cells release GABA to control the synaptic transmission in the retina. Horizontal cells receive direct input from photoreceptors and respond with a negative feedback to cone and rod photoreceptors (Thoreson et al, 2008). They also mediate the responses of the surrounding receptive field of bipolar cells.…”

Ablation of Retinal Horizontal Cells from Adult Mice Leads to Rod Degeneration and Remodeling in the Outer Retina

“…Flat contacts (basal junctions) are formed by OFF bipolar cell dendrites contacting the photoreceptor base , whereas triad synapses consist of a presynaptic ribbon (the specialized glutamate release machinery of photoreceptors) and three postsynaptic elements: two lateral horizontal cell dendrites and one or two centrally oriented ON bipolar cell dendrites (Rao-Mirotznik et al, 1995). At these highly specialized synapses, signal transmission between photoreceptors and horizontal cells is reciprocal: horizontal cells receive input from photoreceptors via ionotropic glutamate receptors (GluRs) and feed positive (Jackman et al, 2011) and negative signals back to cones (Kamermans et al, 2001;Vessey et al, 2005) and rods (Thoreson et al, 2008), thereby regulating photoreceptor output.…”