Expectation violations produce error signals in mouse V1

Abstract

Repeated exposure to visual sequences changes the form of evoked activity in the primary visual cortex (V1). Predictive coding theory provides a potential explanation for this, namely that plasticity shapes cortical circuits to encode spatiotemporal predictions and that subsequent responses are modulated by the degree to which actual inputs match these expectations. Here we use a recently developed statistical modeling technique called Model-Based Targeted Dimensionality Reduction (MbTDR) to study visually-evoked dynamics in mouse V1 in context of a previously described experimental paradigm called "sequence learning". We report that evoked spiking activity changed significantly with training, in a manner generally consistent with the predictive coding framework. Neural responses to expected stimuli were suppressed in a late window (100-150ms) after stimulus onset following training, while responses to novel stimuli were not. Omitting predictable stimuli led to increased firing at the expected time of stimulus onset, but only in trained mice. Substituting a novel stimulus for a familiar one led to changes in firing that persisted for at least 300ms. In addition, we show that spiking data can be used to accurately decode time within the sequence. Our findings are consistent with the idea that plasticity in early visual circuits is involved in coding spatiotemporal information.

Efficient Temporal Coding in the Early Visual System: Existing Evidence and Future Directions

“…This result could reflect the fact that local field potentials largely represent synaptic currents in the dendrites (e.g., inputs) rather than neural spiking (e.g., outputs, Katzner et al, 2009 ). In more recent experiments in our lab, we have found that expectation-violating stimuli tend to elicit more spiking activity ( Price et al, 2022 ). In addition to this unsupervised learning paradigm, there is also evidence for timing information in V1 following reinforcement learning ( Shuler and Bear, 2006 ; Hangya and Kepecs, 2015 ; Levy et al, 2017 ).…”

Repeated passive visual experience modulates spontaneous and non-familiar stimuli-evoked neural activity

“…The internal model could serve as the knowledge of familiarity, and their inhibitory influence on familiar stimulus responsiveness may contribute to novelty detection. Consistently, deviation from or memory of expected sensory experience has been shown to modulate neuronal activity in the visual cortex 30,38,59,[62][63][64][65][66][67][68][69] .…”

Prediction mismatch responses arise as corrections of a predictive spiking code

“…To separate these two effects, subsequent experiments went beyond the oddball paradigm and employed stimuli that become predictable only given a wider context. These experiments showed that also without stimulus adaptation neurons can show strong prediction mismatch responses (PMRs) [6, 7, 8, 9, 10, 11, 12]. While it is still a matter of ongoing research how exactly PMRs arise, they often seem to be modulated by top-down inputs to the cortical circuits [4, 13, 14, 15].…”