Ubiquitous predictive processing in the spectral domain of sensory cortex

The appearance at the anatomical level of a canonical laminar microcircuit suggests that each six-layer column of granular cortex may mediate a canonical computation. Hypotheses for such computations include predictive coding, predictive routing, efficient coding, and others. However, single-neuron recordings capture only the individual elements of the hypothesized laminar microcircuit, while local field potentials (LFPs) from a laminar probe offer insight into the broader population activity. Through the Allen Institutes OpenScope Brain Observatory, data in mice performing a visual oddball task during multi-area laminar recording was used to test predictive processing hypotheses in the spectral domain. Histological labeling of the cortical laminae enabled a fine-grained examination of their roles in the task, and frequency bands capturing both feedforward and feedback effects were analyzed. {gamma}-band local-field potential (LFP) oscillations conveyed feedforward prediction errors in lower sensory areas of cortex; /{beta}-band oscillations weakened in unpredictable conditions compared to predictable ones; and {theta}-band oscillations additionally signalled slower, longer-scale temporal prediction errors. In combination with the previous findings, predictive routing explains these experiments where neither ubiquitous predictive coding nor feedforward adaptation can. SignificanceCortical columns robustly signal perceptual features through the firing rates of spiking neurons. In accordance with this rate coding, predictive processing theories hypothesized that neuronal firing rates ubiquitously signal surprise. However, a recent large-scale study of spike rates did not support this conjecture. An alternate model, predictive routing, suggests that neuronal oscillations rather than spike rates could encode surprise. These neuronal oscillations, which can affect the timing but not rate of spiking, formed coherent {gamma} rhythms which consistently signaled both simpler and more complex forms of surprise in mouse visual cortex. Together with the findings on spike-rates in the same experiment, our findings suggest that cortical circuits encode surprise in the rhythmic timing of spikes rather than in their rate.