Effects of Remote Stimulation on the Modulated Activity of Cat Retinal Ganglion Cells

Abstract

The output of retinal ganglion cells depends on local and global aspects of the visual scene. The local receptive field is well studied and classically consists of a linear excitatory center and a linear antagonistic surround. The global receptive field contains pools of nonlinear subunits that are distributed widely across the retina. The subunit pools mediate in uncertain ways various nonlinear behaviors of ganglion cells, like temporal-frequency doubling, saccadic suppression, and contrast adaptation. To clarify mechanisms of subunit function, we systematically examined the effect of remote grating patterns on the spike activity of cat X-and Y-type ganglion cells in vivo. We present evidence for two distinct subunit types based on spatiotemporal relationships between response nonlinearities elicited by remote drifting and contrast-reversing gratings. One subunit type is excitatory and activated by gratings of ϳ0.1 cycles per degree, while the other is inhibitory and activated by gratings of ϳ1 cycle per degree. The two subunit pools contribute to a global gain control mechanism that differentially modulates ganglion cell response dynamics, particularly for ON-center cells, where excitatory and inhibitory subunit stimulation respectively makes responses to antipreferred and preferred contrast steps more transient. We show that the excitatory subunits also have a profound influence on spatial tuning, turning cells from lowpass into bandpass filters. Based on difference-of-Gaussians model fits to tuning curves, we attribute the increased bandpass selectivity to changes in center-surround strength and relative phase and not center-surround size. A conceptual model of the extraclassical receptive field that could explain many observed phenomena is discussed.

Specific Wiring of Distinct Amacrine Cells in the Directionally Selective Retinal Circuit Permits Independent Coding of Direction and Size

“…We hypothesized an inhibitory receptive field comprised of nonlinear rectifying subunits (Olveczky et al, 2003;Passaglia et al, 2009; Takeshita and Gollisch, 2014) produces a tonic inhibition (0 delay), as individual subunits are asynchronously activated by different phases of the grating (Zaghloul et al, 2007). Indeed, we found that surround inhibition is largely independent of spatial frequency, when stimuli were larger than a certain size (bar width of $75 mm; Figure S7), a characteristic feature of nonlinear surround mechanisms (Olveczky et al, 2003;Hochstein and Shapley, 1976).…”

Encoding visual information in retinal ganglion cells with prosthetic stimulation

“…In addition to the classic center and surround, a subset of parasol cells have an additional response mechanism referred to as nonlinear subunits (Benardete and Kaplan 1999; Victor 1999). These subunits are the defining feature of Y-type ganglion cells in lower mammals (Hochstein and Shapley 1976; Gollisch and Meister 2010), causing the ganglion cell to spike in response to the movement of any textured pattern through the receptive field, including the movement of high-spatial frequency stimuli that could not be resolved by the classical center and surround (Passaglia et al 2009). Taken together, these properties allow midget and parasol cells to encode distinct features of the visual scene; midget cells convey information on fine spatial detail while parasol cells are well-suited for motion analysis (Kaplan and Benardete 2001) (for a discussion on color vision, see Section 4.5).…”

The Effect of Attention on Neuronal Responses to High and Low Contrast Stimuli

“…Simple gain changes of the sort embodied in response gain are seen throughout the brain, including peripheral structures such as the retina (Passaglia et al 2009), raising the possibility that attention uses mechanisms that are similar in form to those used in purely sensory or motor processing. However, experiments comparing the effects of attention on stimuli of different contrasts have described an additional effect (Li and Basso 2008;Martinez-Trujillo and Treue 2002;Reynolds et al 2000).…”