Neurons in the superficial layers of the midbrain superior colliculus
(SC) exhibit distinct tuning properties for visual stimuli, but, unlike
neurons in the geniculocortical visual pathway, most respond best to
visual stimuli that are smaller than the classical receptive field (RF).
The mechanism underlying this size selectivity may depend on the number
and pattern of feedforward retinal inputs and/or the balance between
inhibition and excitation within the RF. We have previously shown that
chronic blockade of NMDA receptors (NMDA-R), which increases the
convergence of retinal afferents onto SC neurons, does not alter size
selectivity in the SC. This suggests that the number of retinal inputs
does not determine size selectivity. Here we show, using single unit
extracellular recordings from the SC of normal hamsters, that size
selectivity in neurons selective for small stimulus size is correlated
with the strength of inhibition within the RF. We also show that dark
rearing causes concomitant reductions in both inhibition and size
selectivity. In addition, dark rearing increases the percentage of neurons
non-selective for stimulus size. Finally, we show that chronic blockade of
NMDA-R, a procedure that does not alter size tuning, also does not change
the strength of inhibition within the RF. Taken together, these results
argue that inhibition within the RF underlies selectivity for small
stimulus size and that inhibition must be intact for size tuning to be
preserved after developmental manipulations of activity. In addition,
these results suggest that regulation of the balance between excitation
and inhibition within the RF does not require NMDA-R activity but does
depend on visual experience. These results suggest that developmental
experience influences neural response properties through an alteration of
inhibitory circuitry.