A neural theory of retino-cortical dynamics

Abstract

As a result of a variety of factors—the movements of the eyes, those of external objects, integration time, vergence, accommodation, and nonuniform retinal sampling—the retinal encoding is highly transient, blurred, and distorted. Yet this problem received very little attention, for most of the models proposed in the literature are built around the analysis of static (or steady-state) and uniformly focused images. Thus, a fundamental problem in visual perception consists of the understanding of the processes underlying the synthesis of phenomenally static, sharp percepts from transient, blurred activities. We present a continuous-time neural theory that proposes two major roles for the retinal transient activity: First, we propose that the nonmonotonic behavior of retinal neurons serves as a simple form of memory that adaptively filters visual signals to guide attentional mechanisms. Second, we propose that the transient activity is essential in achieving sharp dynamic percepts while preserving a good sensitivity to light. Theoretical analysis shows that an extraretinal on-center off-surround feedback anatomy is required to sharpen the “blurred output” from the retinal level. Mathematical properties of such feedback loops indicate that a transient reset mechanism is necessary to avoid smearing. It is proposed that transient retinal cells realize the reset by sending inhibitory signals to sustained activity distributions at higher levels (extraretinal areas: e.g., lateral geniculate nucleus (LGN) and/or visual cortical areas). In this theoretical framework, the continuous time behavior of the visual system can be analyzed in three major phases. In the first phase, sustained retinal signals are sharpened by feedback dominant extra-retinal loops. When the input moves, a second phase is engaged. In this phase, transient retinal cells reset rapidly and briefly extra-retinal activities. In the third phase, extra-retinal loops enter a feedforward mode thereby transferring a faithful copy of retinal activity into their own cells. The feedforward mode is maintained by the transient components of the retinal sustained units. When retinal units enter their steady-state mode, the overall system returns to the first phase where sharpening occurs through feedback dominant extra-retinal loops. The predictions of the theory are compared with various experimental data with emphasis on masking and motion deblurring phenomena.