Ambient Illumination Toggles a Neuronal Circuit Switch in the Retina and Visual Perception at Cone Threshold

Abstract

Gradual changes in the sensory environment can lead to abrupt changes in brain computations and perception. However, mechanistic understanding of the mediating microcircuits is missing. By sliding through light levels from starlight to daylight, we identify retinal ganglion cell types in the mouse that abruptly and reversibly switch the weighting of center and surround interactions in their receptive field around cone threshold. Two-photon-targeted recordings and genetic and viral tracing experiments revealed that the circuit element responsible for the switch is a large inhibitory neuron that provides direct inhibition to ganglion cells. Our experiments suggest that weak excitatory input via electrical synapses together with the spiking threshold in inhibitory cells act as a switch. We also reveal a switch-like component in the spatial integration properties of human vision at cone threshold. This work demonstrates that circuits in the retina can quickly and reversibly switch between two distinct states, implementing distinct perceptual regimes at different light levels.

Function and Circuitry of VIP+ Interneurons in the Mouse Retina

“…The program and methods used were similar to those described previously (Manookin et al, 2008;Farrow et al, 2013;Sümbül et al, 2014). Labeled VIP ϩ cell dendrites and the ChAT bands were imaged using the 40ϫ objective.…”

Ambient illumination switches contrast preference of specific retinal processing streams

“…1) at five different mean light levels (1 R*·rod Ϫ1 ·s Ϫ1 , or 1 R* for short, 10 R*, 100 R*, 1,000 R*, 10,000 R*) and recorded responses of large ensembles of RGCs on MEAs. Stimulation at 1 R* and 10 R* activates only rod photoreceptors (scotopic light levels), with signals elicited at 1 R* being transmitted exclusively by RBCs; stimulation at 100 R* and 1,000 R* activates both rods and cones (mesopic light levels); and stimulation at 10,000 R* activates primarily cones (photopic light level) (Bloomfield and Dacheux 2001;Farrow et al 2013;Field et al 2009;Murphy and Rieke 2006;Naarendorp et al 2010;Szikra et al 2014;Tikidji-Hamburyan et al 2015).…”

“…Similarly, cones can function as relay cells of rod signals at dim light levels (Nelson 1977;Schneeweis and Schnapf 1995;Soucy et al 1998;Szikra et al 2014). AII amacrine cells switch their excitatory input from chemical synapses with rod bipolar cells (RBCs) to electrical synapses with ON cone bipolar cells (Manookin et al 2008;Munch et al 2009), whereas RBCs and some RGCs change the source of their inhibitory input (Farrow et al 2013;Ichinose and Lukasiewicz 2012). The primary rod pathway, rather than saturating, appears to shift from photon counting to contrast encoding with increasing luminance (Ke et al 2014), and synaptic transmission from bipolar cells transitions from a linear to a rectified regime (Grimes et al 2014).…”

“…Basic features of visual scenes (e.g., contrast) are encoded in a distributed manner across RGC types, whereas more elaborate features (e.g., motion direction, movement of an object relative to its background) are selectively detected by a few RGC types. Luminance-dependent changes in chromatic, temporal, and spatial tuning of RGCs were identified early in the history of retinal physiology (Barlow et al 1957;Creutzfeldt and Sakmann 1969;Enroth-Cugell and Lennie 1975;Enroth-Cugell and Robson 1966;Ogawa et al 1966;Reitner et al 1991) and have been analyzed in detail since (Farrow et al 2013;Field et al 2009;Grimes et al 2014). By comparison, how contrast encoding and the detection of complex features depend on ambient illumination is not well studied.…”

Modulation of Fast Narrowband Oscillations in the Mouse Retina and dLGN According to Background Light Intensity

“…Within this natural range, the statistics of photon noise, transitions between rod and cone photoreception, and changes in photoreceptor response kinetics mean that the quality and quantity of visual information available to the brain change substantially. Accordingly, the output of the early visual system changes quantitatively (Barlow et al, 1957;Bisti et al, 1977) and qualitatively (Farrow et al, 2013;Grimes et al, 2014;Odermatt et al, 2012;Tikidji-Hamburyan et al, 2015) as a function of irradiance. So far, these changes have been described mainly at the single-neuron (Barlow et al, 1957;Bisti et al, 1977;Tikidji-Hamburyan et al, 2015) or synaptic level (Farrow et al, 2013;Grimes et al, 2014;Odermatt et al, 2012), while the impact of changing irradiance on the regime of network activity is not well understood.…”