Automatic Adaptation to Fast Input Changes in a Time-Invariant Neural Circuit

Neurons must faithfully encode signals that can vary over many orders of magnitude despite having only limited dynamic ranges. For a correlated signal, this dynamic range constraint can be relieved by subtracting away components of the signal that can be predicted from the past, a strategy known as predictive coding, that relies on learning the input statistics. However, the statistics of input natural signals can also vary over very short time scales e.g., following saccades across a visual scene. To maintain a reduced transmission cost to signals with rapidly varying statistics, neuronal circuits implementing predictive coding must also rapidly adapt their properties. Experimentally, in different sensory modalities, sensory neurons have shown such adaptations within 100 ms of an input change. Here, we show first that linear neurons connected in a feedback inhibitory circuit can implement predictive coding. We then show that adding a rectification nonlinearity to such a feedback inhibitory circuit allows it to automatically adapt and approximate the performance of an optimal linear predictive coding network, over a wide range of inputs, while keeping its underlying temporal and synaptic properties unchanged. We demonstrate that the resulting changes to the linearized temporal filters of this nonlinear network match the fast adaptations observed experimentally in different sensory modalities, in different vertebrate species. Therefore, the nonlinear feedback inhibitory network can provide automatic adaptation to fast varying signals, maintaining the dynamic range necessary for accurate neuronal transmission of natural inputs.Author Summary: An animal exploring a natural scene receives sensory inputs that vary, rapidly, over many orders of magnitude. Neurons must transmit these inputs faithfully despite both their limited dynamic range and relatively slow adaptation time scales. One well-accepted strategy for transmitting signals through limited dynamic range channels–predictive coding–transmits only components of the signal that cannot be predicted from the past. Predictive coding algorithms respond maximally to unexpected inputs, making them appealing in describing sensory transmission. However, recent experimental evidence has shown that neuronal circuits adapt quickly, to respond optimally following rapid input changes. Here, we reconcile the predictive coding algorithm with this automatic adaptation, by introducing a fixed nonlinearity into a predictive coding circuit. The resulting network automatically “adapts” its linearized response to different inputs. Indeed, it approximates the performance of an optimal linear circuit implementing predictive coding, without having to vary its internal parameters. Further, adding this nonlinearity to the predictive coding circuit still allows the input to be compressed losslessly, allowing for additional downstream manipulations. Finally, we demonstrate that the nonlinear circuit dynamics match responses in both auditory and visual neurons. Therefore, we believe that this nonlinear circuit may be a general circuit motif that can be applied in different neural circuits, whenever it is necessary to provide an automatic improvement in the quality of the transmitted signal, for a fast varying input distribution.