Inhibitory plasticity underlies visual deprivation-induced loss of receptive field refinement in the adult superior colliculus

Increasing evidence shows that sensory experience is not necessary for initial patterning of neural circuitry but is essential for maintenance and plasticity. We have investigated the role of visual experience in development and plasticity of inhibitory synapses in the retinocollicular pathway of an altricial rodent, the Syrian hamster. We reported previously that visual receptive field (RF) refinement in superior colliculus (SC) occurs with the same time course in long-term dark-reared (LTDR) as in normally-reared hamsters, but RFs in LTDR animals become unrefined in adulthood. Here we provide support for the hypothesis that this failure to maintain refined RFs into adulthood results from inhibitory plasticity at both pre- and postsynaptic levels. Iontophoretic application of gabazine, a GABA(A) receptor antagonist, or muscimol, a GABA(A) receptor agonist, had less of an effect on RF size and excitability of adult LTDR animals than in short-term DR animals or normal animals. Consistent with these physiological observations, the percentage of GABA-immunoreactive neurons was significantly decreased in the SC of LTDR animals compared to normal animals and to animals exposed to a normal light cycle early in development, before LTDR. Thus GABAergic inhibition in the SC of LTDR animals is reduced, weakening the inhibitory surround and contributing significantly to the visual deprivation-induced enlargement of RFs seen. Our results argue that early visually-driven activity is necessary to maintain the inhibitory circuitry intrinsic to the adult SC and to protect against the consequences of visual deprivation.