Critical and maximally informative encoding between neural populations in the retina

Abstract: Computation in the brain involves multiple types of neurons, yet the organizing principles for how these neurons work together remain unclear. Information theory has offered explanations for how different types of neurons can optimize the encoding of different stimulus features. However, recent experiments indicate that separate neuronal types exist that encode the same stimulus features, but do so with different thresholds. Here we show that the emergence of these types of neurons can be quantitatively described by the theory of transitions between different phases of matter. The two key parameters that control the separation of neurons into subclasses are the mean and standard deviation of noise levels among neurons in the population. The mean noise level plays the role of temperature in the classic theory of phase transitions, whereas the standard deviation is equivalent to pressure, in the case of liquid-gas transitions, or to magnetic field for magnetic transitions. Our results account for properties of two recently discovered types of salamander OFF retinal ganglion cells, as well as the absence of multiple types of ON cells. We further show that, across visual stimulus contrasts, retinal circuits continued to operate near the critical point whose quantitative characteristics matched those expected near a liquid-gas critical point and described by the nearest-neighbor Ising model in three dimensions. By operating near a critical point, neural circuits can optimize the trade-off between maximizing information transmission in a given environment and quickly adapting to a new environment.