Content-based dissociation of hippocampal involvement in prediction

Abstract It has recently become clear that one of the key functions of the hippocampus is to predict future inputs. In line with this, previous research has revealed prediction-related signals in the hippocampus for complex visual objects, such as fractals and abstract shapes. Based on this, it has been suggested that the hippocampus may generate perceptual expectations, especially when relying on rapidly learned predictive associations between arbitrary stimuli. However, it is currently unknown whether the hippocampus implements general-purpose computations that subserve all associative predictions, regardless of stimulus properties, or whether the involvement of the hippocampus is stimulus-dependent. To investigate this, we exposed male and female human participants to complex auditory cues predicting either the shape of a complex object (Experiment 1) or the orientation of a simple line grating (Experiment 2). We measured brain activity using high-resolution functional magnetic resonance imaging (fMRI), in combination with inverted encoding models to reconstruct shape and orientation representations in visual cortex and the hippocampus. Our results revealed that expectations about shape and orientation evoked distinct representations in the hippocampus. For complex shapes, the hippocampus represented which shape was expected, potentially serving as a source of top-down predictions. In contrast, for simple gratings, the hippocampus represented only unexpected orientations, more reminiscent of a prediction error. We discuss several potential explanations for this dissociation, concluding that the computational role of the hippocampus in predictive processing depends upon the nature and complexity of stimuli. Significance Statement To deal with the noisy and ambiguous sensory signals received by our brain, it is crucial to use prior knowledge of the world to guide perception. Previous research suggests that the hippocampus is involved in predicting upcoming visual stimuli based on prior knowledge. In the current study, we show that hippocampal prediction is specific to expectations of complex objects, whereas for simple features the hippocampus generates an opposite prediction error signal instead. These findings demonstrate that the computational role of the hippocampus can be content-sensitive and refine our understanding of the involvement of memory systems in predictive processing.