The image on the retina is almost never static. Eye, head, and body
movements, and externally generated motion create rapid and continual
changes in the retinal image (“active vision”). Virtually all
vision in animals such as primates, which make saccades as often as
3–4 times/s, is based on information that must be derived from
the first few hundred milliseconds after sudden, global changes in the
retinal image. These changes may be accompanied by large changes in area
mean luminance, as well as higher order image contrast statistics. This
study investigated how retinal ganglion cell responses, whose response
properties have been typically studied and defined in a stable stimulus
regime, are affected by sudden changes in mean luminance that are
characteristic of active vision. Specifically, the steady-state responses
of retinal ganglion cells to static or moving square-wave grating stimuli
were recorded in an isolated, superfused rabbit eyecup preparation and
compared to responses after saccade-like changes in luminance. The manner
of coding after luminance changes was different for different ganglion
cell classes; both suppression and enhancement of responses to patterns
following luminance changes were found. Brisk-transient Off cells
unambiguously signaled the darkening of the overall image, but were also
modulated by the subsequently appearing grating stimulus. Several types of
On-center cell behavior were observed, ranging from strong suppression of
the subsequent response by luminance changes, to strong enhancement.
Overall, most ganglion cells distinguished static patterns after a
luminance change via differences in their spike discharges nearly
as well as before, although there were clear asymmetries between the On
and Off pathways. Changes in mean luminance in some ganglion cells, such
as On–Off directionally selective ganglion cells, could create large
phase shifts in the response to patterned, moving stimuli, although these
stimuli were still detected immediately after luminance changes. The
results of this study show that the image dynamics of active vision may be
a fundamental challenge for the visual system because of strong effects on
retinal ganglion cell function. However, rapid extraction of unambiguous
information after luminance changes appears to be encoded in differences
in the spike discharges in different retinal ganglion cell classes.
Asymmetries among ganglion cell classes in sensitivity to luminance
changes may provide a basis by which some provide the
“context” for interpreting the firing of others.
Divisive suppression explains high-precision firing and contrast adaptation in retinal ganglion cells