Roles of ON Cone Bipolar Cell Subtypes in Temporal Coding in the Mouse Retina

Abstract

In the visual system, diverse image processing starts with bipolar cells, which are the second-order neurons of the retina. Thirteen subtypes of bipolar cells have been identified, which are thought to encode different features of image signaling and to initiate distinct signal-processing streams. Although morphologically identified, the functional roles of each bipolar cell subtype in visual signal encoding are not fully understood. Here, we investigated how ON cone bipolar cells of the mouse retina encode diverse temporal image signaling. We recorded bipolar cell voltage changes in response to two different input functions: sinusoidal light and step light stimuli. Temporal tuning in ON cone bipolar cells was diverse and occurred in a subtype-dependent manner. Subtypes 5s and 8 exhibited low-pass filtering property in response to a sinusoidal light stimulus, and responded with sustained fashion to step-light stimulation. Conversely, subtypes 5f, 6, 7, and XBC exhibited bandpass filtering property in response to sinusoidal light stimuli, and responded transiently to step-light stimuli. In particular, subtypes 7 and XBC were high-temporal tuning cells. We recorded responses in different ways to further examine the underlying mechanisms of temporal tuning. Current injection evoked low-pass filtering, whereas light responses in voltage-clamp mode produced bandpass filtering in all ON bipolar cells. These findings suggest that cone photoreceptor inputs shape bandpass filtering in bipolar cells, whereas intrinsic properties of bipolar cells shape low-pass filtering. Together, our results demonstrate that ON bipolar cells encode diverse temporal image signaling in a subtype-dependent manner to initiate temporal visual information-processing pathways.

Functional Circuitry of the Retina

“…A recent study revealed distinct postsynaptic temporal processing characteristics of different ON bipolar cell types (Ichinose et al 2014). Experiments combining light responses and current injection suggested that low-pass characteristics (i.e., suppression of high temporal frequencies) depended on intrinsic properties of the bipolar cells, whereas high-pass characteristics (i.e., suppression of low temporal frequencies) were generated through synaptic mechanisms.…”

“…The nonlinearity of glutamate release is most striking in laminae near the middle of the IPL, adjacent to the boundary between ON and OFF layers (Roska & Werblin 2001, Baden et al 2013, Borghuis et al 2013, Ichinose et al 2014). Because each bipolar cell subunit is small, it is stimulated by high spatial frequencies; the independent activity of each subunit endows the postsynaptic ganglion cell with sensitivity to fine spatial patterns (Demb et al 2001, Baccus et al 2008, Schwartz et al 2012).…”

“Silent” NMDA Synapses Enhance Motion Sensitivity in a Mature Retinal Circuit

“…To achieve such presynaptic balance, glutamate release from bipolar cells onto DSGCs must be curbed until stimuli are sufficiently strong to evoke GABA release from starbursts. This is thought to be accomplished by using high- and low-sensitivity bipolar cells (Ichinose et al, 2014; Odermatt et al, 2012; Poleg-Polsky and Diamond, 2016b) to independently drive starbursts and DSGCs, in a way that compensates for the starburst's threshold non-linearity (Figure 1A & B) (Poleg-Polsky and Diamond, 2016b). As this model requires the matching of presynaptic GABA/glutamate/ACh signals, we refer to it as the ‘matched’ model for DS in ganglion cells.…”

Marking Cells with Infrared Fluorescent Proteins to Preserve Photoresponsiveness in the Retina

“…The experimental techniques were similar to those described previously (13,14). The eyes were placed in a cooled oxygenated dissecting solution containing 115 mM NaCl, 2.5 mM KCl, 2.5 mM CaCl 2 , 1.0 mM MgCl 2 , 10 mM HEPES, and 28 mM glucose, and were adjusted to pH 7.4 with NaOH.…”