Ambient illumination switches contrast preference of specific retinal processing streams

Pearson, James T.; Kerschensteiner, Daniel

doi:10.1152/jn.00360.2015

Cited by 38 publications

(35 citation statements)

References 59 publications

(78 reference statements)

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“…Previous work has shown that ooDSGCs are typically dominated by OFF responses at high light levels and prefer ON responses at lower light levels (Pearson and Kerschensteiner, 2015). Similarly, our results indicate that the OFF subfields become much smaller than the ON subfields under scotopic conditions (Fig 2, Fig 4B).…”

Section: Gabaa Antagonists Reduce Sensitivity Difference and Increasesupporting

confidence: 85%

“…First, under photopic conditions, ooDSGCs exhibit roughly equal responses to objects brighter or dimmer than the background. However, under scotopic conditions, they lose their 'OFF' response and respond primarily to increments of light (Pearson and Kerschensteiner, 2015). The second identified form of adaptation is a broadening of direction tuning among superior-preferring (s-)DSGCs at low light levels: the other three ooDSGC types preserve their tuning widths across light levels (Yao et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

Yao

Field

2019

Preprint

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Information about motion is encoded by direction-selective retinal ganglion cells (DSGCs). These cells reliably transmit this information across a broad range of light levels, spanning moonlight to sunlight. Previous work indicates that adaptation to low light levels causes heterogeneous changes to the direction tuning of ON-OFF (oo)DSGCs and suggests that superiorpreferring ON-OFF DSGCs (s-DSGCs) are biased toward detecting stimuli rather than precisely signaling direction. Using a large-scale multi-electrode array, we measured the absolute sensitivity of ooDSGCs and found that s-DSGCs are ten-fold more sensitive to dim flashes of light than other ooDSGCs. We measured their receptive field sizes and found that s-DSGCs also have larger receptive fields than other ooDSGCs, however, the size difference does not fully explain the sensitivity difference. Using a conditional knockout of gap junctions and pharmacological manipulations, we demonstrate that GABA-mediated inhibition contributes to the difference in absolute sensitivity and receptive field size at low light levels, while the connexin36-mediated gap junction coupling plays a minor role. We further show that GABA-mediated inhibition masks the OFF response of ooDSGCs under scotopic conditions, restricting their responses to increases in light. These results reveal that GABAergic inhibition controls and differentially modulates the responses of ooDSGCs under scotopic conditions. Significance StatementLight adaptation and parallel processing are two major functions of retina. Here we show that parallel processing is differentially regulated between photopic and scotopic conditions across DSGCs. This differential adaptation alters the absolute sensitivity and RF size of s-DSGCs relative to other ooDSGC types. These results point to novel mechanisms and possibly new circuit elements that shape retinal processing of motion under rod-mediated light levels.

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Section: Gabaa Antagonists Reduce Sensitivity Difference and Increasesupporting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

Yao

Field

2019

Preprint

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“…Recent studies illustrate, albeit qualitatively, how little we understand about the behaviors of some cell types in response to changing ambient light intensities. Across ~100-fold changes in background light level, some ON or OFF cells seemed to alter their identities and generate ON–OFF responses (Pearson & Kerschensteiner 2015, Tikidji-Hamburyan et al 2015). These effects were also observed in vivo.…”

Section: Resultsmentioning

confidence: 99%

Functional Circuitry of the Retina

Demb

Singer

2015

Annu. Rev. Vis. Sci.

154

131

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The mammalian retina is an important model system for studying neural circuitry: Its role in sensation is clear, its cell types are relatively well defined, and its responses to natural stimuli—light patterns—can be studied in vitro. To solve the retina, we need to understand how the circuits pre-synaptic to its output neurons, ganglion cells, divide the visual scene into parallel representations to be assembled and interpreted by the brain. This requires identifying the component interneurons and understanding how their intrinsic properties and synapses generate circuit behaviors. Because the cellular composition and fundamental properties of the retina are shared across species, basic mechanisms studied in the genetically modifiable mouse retina apply to primate vision. We propose that the apparent complexity of retinal computation derives from a straightforward mechanism—a dynamic balance of synaptic excitation and inhibition regulated by use-dependent synaptic depression—applied differentially to the parallel pathways that feed ganglion cells.

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“…For example, neurons in the piriform cortex represent odor identity while remaining invariant to its exact concentration (Bolding and Franks, 2018). Similarly, neurons in the visual cortex can keep the same orientation tuning curve over different contrasts (Sclar and Freeman, 1982).In the retina, direction selective (DS) ganglion cells (GC) respond selectively to a motion direction in different contexts such as different backgrounds (Chen et al, 2016), different natural scenes (Im and Fried, 2016), and over a broad range of luminosities (Pearson and Kerschensteiner, 2015; Vaney et al, 2001;Yao et al, 2018). Switching the average luminance from dim to bright light will change the dominant circuits that convey visual information inside the retina, leading to major changes in the responses of ganglion cells (Pearson and Kerschensteiner, 2015;Wässle, 2004).…”

mentioning

confidence: 99%

“…In the retina, direction selective (DS) ganglion cells (GC) respond selectively to a motion direction in different contexts such as different backgrounds (Chen et al, 2016), different natural scenes (Im and Fried, 2016), and over a broad range of luminosities (Pearson and Kerschensteiner, 2015; Vaney et al, 2001;Yao et al, 2018). Switching the average luminance from dim to bright light will change the dominant circuits that convey visual information inside the retina, leading to major changes in the responses of ganglion cells (Pearson and Kerschensteiner, 2015;Wässle, 2004). For example, cells will change their ON-OFF polarity (Tikidji-Hamburyan et al, 2015).…”

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confidence: 99%

All-optical interrogation of a direction selective retinal circuit by holographic wave front shaping

Spampinato

Ronzitti

Zampini

et al. 2019

Preprint

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Direction selective (DS) ganglion cells (GC) in the retina maintain their tuning across a broad range of light levels. Yet very different circuits can shape their responses from bright to dim light, and their respective contributions are difficult to tease apart. In particular, the contribution of the rod bipolar cell (RBC) primary pathway, a key player in dim light, is unclear. To understand its contribution to DSGC response, we designed an all-optical approach allowing precise manipulation of single retinal neurons. Our system activates single cells in the bipolar cell (BC) layer by two-photon (2P) temporally focused holographic illumination, while recording the activity in the ganglion cell layer by 2P Ca 2 imaging. By doing so, we demonstrate that RBCs provide an asymmetric input to DSGCs, suggesting they contribute to their direction selectivity. Our results suggest that every circuit providing an input to direction selective cells can generate direction selectivity by itself. This hints at a general principle to achieve robust selectivity in sensory areas.A major goal in neuroscience is to understand the circuits that embody the computations performed by sensory neurons. In particular, a striking feature of sensory processing is the ability of neurons to perform the same computation in different contexts. For example, neurons in the piriform cortex represent odor identity while remaining invariant to its exact concentration (Bolding and Franks, 2018). Similarly, neurons in the visual cortex can keep the same orientation tuning curve over different contrasts (Sclar and Freeman, 1982).In the retina, direction selective (DS) ganglion cells (GC) respond selectively to a motion direction in different contexts such as different backgrounds (Chen et al., 2016), different natural scenes (Im and Fried, 2016), and over a broad range of luminosities (Pearson and Kerschensteiner, 2015; Vaney et al., 2001;Yao et al., 2018). Switching the average luminance from dim to bright light will change the dominant circuits that convey visual information inside the retina, leading to major changes in the responses of ganglion cells (Pearson and Kerschensteiner, 2015;Wässle, 2004). For example, cells will change their ON-OFF polarity (Tikidji-Hamburyan et al., 2015). It is therefore particularly striking that direction selectivity remains constant across the ten billion fold change of luminance separating day from night (Yao et al., 2018), despite the involvement of distinct circuits. A major challenge is to understand how this feature is achieved.During daylight conditions, where rods are saturated and cones transmit light input, the major component responsible for direction selectivity is a functional asymmetry. This results either from an asymmetric inhibition or an asymmetric morphology. For example, in the ON-OFF

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Ambient illumination switches contrast preference of specific retinal processing streams

Abstract: Pearson JT, Kerschensteiner D. Ambient illumination switches contrast preference of specific retinal processing streams.

Cited by 38 publications

References 59 publications

Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

Functional Circuitry of the Retina

All-optical interrogation of a direction selective retinal circuit by holographic wave front shaping

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