Contextual Expectations Shape Cortical Reinstatement of Sensory Representations

Abstract

When making a turn at a familiar intersection, we know what items and landmarks will come into view. These perceptual expectations, or predictions, come from our knowledge of the context, however it's unclear how memory and perceptual systems interact to support the prediction and reactivation of sensory details in cortex. To address this, human participants learned the spatial layout of animals positioned in a cross maze. During fMRI, participants of both sexes navigated between animals to reach a target, and in the process saw a predictable sequence of five animal images. Critically, to isolate activity patterns related to item predictions, rather than bottom-up inputs, one quarter of trials ended early, with a blank screen presented instead. Using multivariate pattern similarity analysis, we reveal that activity patterns in early visual cortex, posterior medial regions, and the posterior hippocampus showed greater similarity when seeing the same item compared to different items. Further, item effects in posterior hippocampus were specific to the sequence context. Critically, activity patterns associated with seeing an item in visual cortex and posterior medial cortex, were also related to activity patterns when an item was expected, but omitted, suggesting sequence predictions were reinstated in these regions. Finally, multivariate connectivity showed that patterns in the posterior hippocampus at one position in the sequence were related to patterns in early visual cortex and posterior medial cortex at a later position. Together, our results support the idea that hippocampal representations facilitate sensory processing by modulating visual cortical activity in anticipation of expected items. Significance statementOur visual world is a series of connected events, where we can predict what we might see next based on our recent past. Understanding the neural circuitry and mechanisms of the perceptual and memory systems that support these expectations is fundamental to revealing how we perceive and act in our world. Using brain imaging, we studied what happens when we expect to see specific visual items, and how such expectations relate to top-down memory signals. We find both visual and memory systems reflect item predictions, and moreover, we show that hippocampal activity supports predictions of future expected items. This demonstrates that the hippocampus acts to predict upcoming items, and reinstates such predictions in cortex.

Communication of perceptual predictions from the hippocampus to the deep layers of the parahippocampal cortex

“…We also hypothesised that this representation would be reflected in the subiculum as it travelled from the hippocampus to the cortex [7,8]. Previous research has found a change in the com-plexity of representations along the long axis of the hippocampus [24], and that the posterior hippocampus is involved in signalling perceptual predictions and prediction errors based on simple associations [8,9,25]. Therefore, we predicted that the posterior hippocampus and its subfields would contain information about the expected shape.…”

“…The hippocampus has recently been suggested as an essential region coordinating learning and exploitation of predictive relationships for perceptual inference [3,4]. Representations of predicted stimuli have been found in the hippocampus [5–7], and informational connectivity between the hippocampus and visual cortex increases after an association has been learnt [8,9]. However, with typical fMRI analyses, these studies could not determine whether the hippocampus was re-sponsible for passing these predictions to the cortex.…”

Neural patterns of conscious visual awareness in the Riddoch syndrome

“…Although we did not explicitly address this question, we suspect that the hallucinations observed here are task-induced, in that they may be brought upon by strong expectations about encountering visual motion immediately after the cue at the start of each trial 40 . In fact, several recent reports have proposed that hippocampal neural representations generate cued predictions about upcoming sensory events, modulating activity in sensory cortex in a predominantly top-down fashion [41][42][43][44] .…”

Neural codes track prior events in a narrative and predict subsequent memory for details

“…Previous fMRI studies have identified history-dependent representations in the brain during context-dependent sequence learning tasks (Clarke et al, 2022; Hsieh et al, 2014) but these studies have not sought to discriminate between the three possibilities listed above. The first goal of our study is to test for all three types of history-dependent representation during context-dependent sequence learning.…”