Retinal bipolar cells: Temporal filtering of signals from cone photoreceptors

Burkhardt, Dwight A.; Fahey, Patrick K.; Sikora, Michael

doi:10.1017/s0952523807070630

Cited by 27 publications

(39 citation statements)

References 42 publications

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“…6B, subtype 5s, G, subtype 8). This indicates that the photoreceptor inputs in ON bipolar cells are bandpass filtering in nature, which is consistent with previous findings in the rod pathway (Armstrong-Gold and Rieke, 2003).…”

Section: Search For Underlying Mechanisms Of On Bipolar Cell Responsesupporting

confidence: 82%

“…Diverse visual signal-processing pathways start at the retinal bipolar cell level (Awatramani and Slaughter, 2000;DeVries, 2000;. Several subtypes of ON cone bipolar cells have been identified by morphological studies in the mouse retina (Ghosh et al, 2004;Wässle et al, 2009); however, except for blue cone bipolar cells (Haverkamp et al, 2005), the functions of ON bipolar cells remain poorly understood.…”

Section: Discussionmentioning

confidence: 99%

“…X and Y ganglion cells were characterized as the origins of two separate visual signaling pathways; they respond linearly and nonlinearly to sinusoidal light stimuli and in a sustained and transient fashion to step-pulse light stimuli, respectively (EnrothCugell and Robson, 1966;Cleland et al, 1971). This transient and sustained dichotomy is observed throughout the visual system, from retinal bipolar cells to striate cortical cells (Cleland et al, 1971;Ikeda and Wright, 1974;Awatramani and Slaughter, 2000). Psychophysical experiments further characterized the functions of the two distinct neural pathways: parvocellular (sustained) pathways for encoding color and shape, and magnocellular (transient) pathways for encoding motion (Livingstone andHubel, 1987, 1988).…”

Section: Introductionmentioning

confidence: 99%

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

Ichinose

Fyk‐Kolodziej

Cohn

2014

Journal of Neuroscience

112

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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.

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Section: Search For Underlying Mechanisms Of On Bipolar Cell Responsesupporting

confidence: 82%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Ichinose

Fyk‐Kolodziej

Cohn

2014

Journal of Neuroscience

112

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“…When cones were dialyzed with 20 µM MLCK peptide, responses were shifted to lower frequencies, peaking at 1.7 ± 0.2 Hz (P = 0.002) and having Hz for On BCs (n = 7) and fell off at both higher and lower frequencies, consistent with band-pass properties of photoreceptor synaptic transmission in amphibian retinas (Fig. 9, B and C, black; Armstrong-Gold and Rieke, 2003; Burkhardt et al, 2007). In the presence of 20 µM calmidazolium, responses for all HCs and On BCs peaked at 0.5 Hz, the lowest frequency tested, and were reduced at higher frequencies relative to control conditions (Fig.…”

Section: Synaptic Filtering By Ca 2+ /Cam-dependent Replenishmentmentioning

confidence: 75%

“…Rod and cone synapses function as band-pass filters (Armstrong-Gold and Rieke, 2003;Burkhardt et al, 2007). Although several presynaptic factors, including gap-junctional coupling, voltage-gated conductances, and synaptic release kinetics, likely contribute to this (ArmstrongGold and Rieke, 2003;Zhang and Wu, 2005;Burkhardt et al, 2007;Barrow and Wu, 2009), the role of synaptic vesicle replenishment has not yet been explored.…”

Section: Introductionmentioning

confidence: 99%

Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

Hook¹,

Parmelee²,

Chen³

et al. 2014

J Cell Biol

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At the first synapse in the vertebrate visual pathway, light-evoked changes in photoreceptor membrane potential alter the rate of glutamate release onto second-order retinal neurons. This process depends on the synaptic ribbon, a specialized structure found at various sensory synapses, to provide a supply of primed vesicles for release. Calcium (Ca 2+ ) accelerates the replenishment of vesicles at cone ribbon synapses, but the mechanisms underlying this acceleration and its functional implications for vision are unknown. We studied vesicle replenishment using paired whole-cell recordings of cones and postsynaptic neurons in tiger salamander retinas and found that it involves two kinetic mechanisms, the faster of which was diminished by calmodulin (CaM) inhibitors. We developed an analytical model that can be applied to both conventional and ribbon synapses and showed that vesicle resupply is limited by a simple time constant,  = 1/(Ds), where D is the vesicle diffusion coefficient,  is the vesicle diameter,  is the vesicle density, and s is the probability of vesicle attachment. The combination of electrophysiological measurements, modeling, and total internal reflection fluorescence microscopy of single synaptic vesicles suggested that CaM speeds replenishment by enhancing vesicle attachment to the ribbon. Using electroretinogram and whole-cell recordings of light responses, we found that enhanced replenishment improves the ability of cone synapses to signal darkness after brief flashes of light and enhances the amplitude of responses to higherfrequency stimuli. By accelerating the resupply of vesicles to the ribbon, CaM extends the temporal range of synaptic transmission, allowing cones to transmit higher-frequency visual information to downstream neurons. Thus, the ability of the visual system to encode time-varying stimuli is shaped by the dynamics of vesicle replenishment at photoreceptor synaptic ribbons.

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A single retinal circuit model for multiple computations

Sağlam

Hayashida

2018

Biol Cybern

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Vision is dependent on extracting intricate features of the visual information from the outside world, and complex visual computations begin to take place as soon as at the retinal level. In multiple studies on salamander retinas, the responses of a subtype of retinal ganglion cells, i.e., fast/biphasic-OFF ganglion cells, have been shown to be able to realize multiple functions, such as the segregation of a moving object from its background, motion anticipation, and rapid encoding of the spatial features of a new visual scene. For each of these visual functions, modeling approaches using extended linear-nonlinear cascade models suggest specific preceding retinal circuitries merging onto fast/biphasic-OFF ganglion cells. However, whether multiple visual functions can be accommodated together in a certain retinal circuitry and how specific mechanisms for each visual function interact with each other have not been investigated. Here, we propose a physiologically consistent, detailed computational model of the retinal circuit based on the spatiotemporal dynamics and connections of each class of retinal neurons to implement object motion sensitivity, motion anticipation, and rapid coding in the same circuit. Simulations suggest that multiple computations can be accommodated together, thereby implying that the fast/biphasic-OFF ganglion cell has potential to output a train of spikes carrying multiple pieces of information on distinct features of the visual stimuli.

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Retinal bipolar cells: Temporal filtering of signals from cone photoreceptors

Cited by 27 publications

References 42 publications

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

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

Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

A single retinal circuit model for multiple computations

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