Encoding surprise by retinal ganglion cells

The efficient coding hypothesis posits that early sensory neurons transmit maximal information about sensory stimuli, given internal constraints. A central prediction of this theory is that neurons should preferentially encode stimuli that are most surprising. Previous studies suggest this may be the case in early visual areas, where many neurons respond strongly to rare or surprising stimuli. For example, previous research showed that when presented with a rhythmic sequence of full-field flashes, many retinal ganglion cells (RGCs) respond strongly at the instance the flash sequence stops, and when another flash would be expected. This phenomenon is called the ‘omitted stimulus response’. However, it is not known whether the responses of these cells varies in a graded way depending on the level of stimulus surprise. To investigate this, we presented retinal neurons with extended sequences of stochastic flashes. With this stimulus, the surprise associated with a particular flash/silence, could be quantified analytically, and varied in a graded manner depending on the previous sequences of flashes and silences. Interestingly, we found that RGC responses could be well explained by a simple normative model, which described how they optimally combined their prior expectations and recent stimulus history, so as to encode surprise. Further, much of the diversity in RGC responses could be explained by the model, due to the different prior expectations that different neurons had about the stimulus statistics. These results suggest that even as early as the retina many cells encode surprise, relative to their own, internally generated expectations.Author summary: A long-standing theory suggests that sensory neurons work to transmit as much visual information as possible using little energy. According to this idea, sensory neurons should put most energy into encoding stimuli that are unexpected or surprising. Previous research has shown that this may be true for certain neurons in the retina, that respond strongly when they see something unusual, like a sudden change in a sequence of flashes. Here, to test this theory, we presented the retina with random sequences of light flashes, and measured whether retinal neuron responses correlated with how surprising each flash in the sequence was. Consistent with the theory, we found that retinal neuron responses in our experiment could be explained by a model that assumed that they encode surprise. Moreover, differences between each neuron’s responses could be predicted due to their different expectations about which stimuli were most likely.