ENCODING MECHANISMS BASED ON FAST OSCILLATIONS IN THE RETINA OF THE CAT AND THEIR DEPENDENCIES ON ANESTHESIA
retina, oscillation, synchronization, halothane, visual
Processing in the visual system starts in the retina. Its complex network of cells with different properties enables for parallel encoding and transmission of visual information to the lateral geniculate nucleus (LGN), where information is subsequently processed and transmitted to the cortex. In the retina, it has been shown that responses are often accompanied by fast synchronous oscillations (30 - 90 Hz) in a stimulus-dependent manner. Studies in the frog, cat and monkey, have found that retinal oscillations are very strong for responses to large stimuli and that they probably encode global stimulus properties, such as size and continuity (Neuenschwander and Singer, 1996; Ishikane et al., 2005). Moreover, simultaneous recordings from different levels in the visual system have shown that the oscillatory patterning of retinal ganglion cell responses are transmitted to the cortex via the LGN (Castelo-Branco et al., 1998). Overall these results suggest that feedforward synchronous oscillations contribute to visual encoding. In the present study on the LGN of the anesthetized cat, we further investigate the role of retina oscillations in early visual processing by applying complex stimuli, such as natural visual scenes, light spots of varying size and contrast, and flickering checkerboards. This is a necessary step for understanding encoding mechanisms in more naturalistic conditions, since most data on retinal oscillations have been obtained for responses to simple, flashed and stationary stimuli. Correlation analysis of spiking responses confirmed previous results showing that oscillatory responses in the retina (observed here from the LGN responses) largely depend on the size and stationarity of the stimulus. For natural scenes (full gray-level and binary movies) oscillations appeared only for brief moments when receptive fields were dominated by large continuous, flat-contrast surfaces. Oscillatory activity seemed to be dependent on a critical mass of activated cells suggesting that it arises from large-scale horizontal interactions in the retina. Moreover, our results show that retinal oscillations in the cat are surprisingly dependent on the halothane anesthesia. In the absence of halothane, oscillatory activity vanished independent of the characteristics of the visual stimulus. The same findings were obtained for isoflurane, which has similar pharmacological properties. These new and unexpected results question whether feedfoward oscillations in the early visual system are simply due to an imbalance between excitation and inhibition in the retinal networks generated by the halogenated anesthetics. Further studies in awake behaving animals are necessary to extend these conclusions.