Photic-induced sensitization: eye-specific neural plasticity and effect of behavioral state

We reported previously that exposure to repetitive visual stimulation in ordinary adult rats results in acquisition of an enduring increase in magnitude and change in character of visual cortical responses. This sensitization is consistent with experience-dependent neuroplastic changes, but could also reflect alterations in response with behavioral state during testing. The aim of this study was to distinguish the contributions of behavioral state and neural plasticity in this photic-induced sensitization. We used repetitive light-emitting diode flashes delivered monocularly and recorded electrocorticographically in the albino rat in which retino-geniculo-cortical projections are predominantly crossed. This enabled comparison of visual responses of sensitized visual circuitry associated with one eye to responses from effectively unsensitized circuitry associated with the second eye at similar time points in an animal, thus providing an internal control for behavioral state. Following sensitization, monocular stimulation of one eye produced the characteristic high amplitude driven spike-wave response in corresponding contralateral visual cortex, but not ipsilateral cortex. Expression of the sensitized driven response was optimal in the quiet awake state and suppressed during active exploration, drowsiness, or anesthesia. When the animal was in the quiet awake state, producing sensitized responses to stimulation of the first eye, no such response was observed on alternate trials upon stimulation of the second eye. Only after extended exposure of the second eye did the high amplitude driven spike-wave response in contralateral visual cortex develop. The data further suggest some degree of sensitization of ipsilateral pathways may accompany monocular stimulation and that effects of monocular sensitization could include suppression in pathways related to the unstimulated eye. Thus, while behavioral state influences expression of the sensitized driven visual response, the eye-specific nature of the effect provides strong evidence that response enhancement reflects neuroplasticity in visual pathways and not a more general change in behavioral state during testing.