The Journal of Neuroscience, March 1, 2000, 20(5):1941-1951
Three Levels of Lateral Inhibition: A Space-Time Study of the
Retina of the Tiger Salamander
Botond
Roska,
Erik
Nemeth,
Laszlo
Orzo, and
Frank S.
Werblin
Division of Neurobiology, Department of Molecular and Cell
Biology, University of California at Berkeley, Berkeley,
California 94720
The space-time patterns of activity generated across arrays of
retinal neurons can provide a sensitive measurement of the effects of
neural interactions underlying retinal activity. We measured the
excitatory and inhibitory components associated with these patterns at
each cellular level in the retina and further dissected inhibitory
components pharmacologically. Using perforated and loose patch
recording, we measured the voltages, currents, or spiking at 91 lateral
positions covering ~2 mm in response to a flashed 300-µm-wide bar.
First, we showed how the effect of well known lateral inhibition at the
outer retina, mediated by horizontal cells, evolved in time to compress
the spatial representation of the stimulus bar at ON and OFF bipolar
cell bodies as well as horizontal cells. Second, we showed, for the
first time, how GABAC receptor mediated amacrine cell
feedback to bipolar terminals compresses the spatial representation of
the stimulus bar at ON bipolar terminals over time. Third, we showed
that a third spatiotemporal compression exists at the ganglion cell
layer that is mediated by feedforward amacrine cells via
GABAA receptors. These three inhibitory mechanisms, via
three different receptor types, appear to compensate for the effects of
lateral diffusion of activity attributable to dendritic spread and
electrical coupling between retinal neurons. As a consequence, the
width of the final representation at the ganglion cell level
approximates the dimensions of the original stimulus bar.
Key words:
retina; inhibition; feedback; patch clamp; activity
pattern; GABA
Copyright © 2000 Society for Neuroscience 0270-6474/00/2051941-11$05.00/0