Contrast-dependent response modulation in convolutional neural networks captures behavioral and neural signatures of visual adaptation

Abstract

Human perception is robust under challenging conditions, for example when sensory inputs change over time. Temporal adaptation in the form of reduced responses to repeated external stimuli is ubiquitously observed in the brain, yet it remains unclear how repetition suppression aids recognition of novel inputs. To clarify this, we collected behavioural and electrocorticography (EEG) measurements while human participants categorized objects embedded in visual noise patterns after first viewing these patterns in isolation, inducing adaptation to the noise stimulus. We furthermore manipulated the availability of object information in the visual input by varying the contrast of the noise-embedded objects. Our results provide convergent behavioral, neural and computational evidence of a benefit of temporal adaptation on sensory representations. Adapting to a noise pattern resulted in overall faster object recognition and better recognition of objects as object contrast increased. These adaptation-induced behavioral improvements were accompanied by more pronounced contrast-dependent modulation of object-evoked EEG responses, and better decoding of object information from EEG activity. To identify potential neural computations mediating the benefits of temporal adaptation on object recognition, we equipped task-optimized deep convolutional neural networks (DCNNs) with different candidate mechanisms to adjust network activations over time. DCNNs with intrinsic adaptation mechanisms, such as additive suppression, best captured contrast-dependent human performance benefits, whilst also showing improved object decoding as a result of adaptation. Finally, adaptation effects in networks that use temporal divisive normalization, a biologically-plausible canonical neural computation, were most robust to spatial shifts, suggesting that temporal adaptation via divisive normalization aids stable representations of time-varying visual inputs. Overall, our results demonstrate how temporal adaptation improves sensory representations and identify candidate neural computations mediating these effects. Author summaryRobust perception is essential for the human brain to detect, process, and act upon new sensory inputs. Temporal adaptation is believed to play a key role in robust sensory processing by allowing neurons to continuously adjust their responses to previous inputs in order to optimize the processing of future inputs. Here, we show that temporal adaptation aids visual object recognition by improving neural representations of object contrast and object category. By emulating temporal adaptation in deep convolutional neural network models with different computational mechanisms, we identify candidate neural computations mediating benefits of temporal adaptation on sensory processing.