Abstract
The ability to identify and react to novelty within the environment is fundamental to survival. Computational models emphasize the potential role of the hippocampus in novelty detection, its unique anatomical circuitry making it ideally suited to act as a comparator between past and present experience. The hippocampus, therefore, is viewed to detect associative mismatches between what is expected based on retrieval of past experience and current sensory input. However, direct evidence that the human hippocampus performs such operations is lacking. We explored brain responses to novel sequences of objects using functional magnetic resonance imaging (fMRI), while subjects performed an incidental target detection task. Our results demonstrate that hippocampal activation was maximal when prior predictions concerning which object would appear next in a sequence were violated by sensory reality. In so doing, we establish the biological reality of associative match-mismatch computations within the human hippocampus, a process widely held to play a cardinal role in novelty detection. Our results also suggest that the hippocampus may generate predictions about how future events will unfold, and critically detect when these expectancies are violated, even when task demands do not require it. The present study also offers broader insights into the nature of essential computations carried out by the hippocampus, which may also underpin its unique contribution to episodic memory.
Highlights
We have all had the experience of walking into a familiar place, for example our living room, and immediately noticing that a new object such as a painting is present, or that the furniture has been rearranged
How might the brain enable us to rapidly and apparently effortlessly detect such unexpected occurrences, when familiar objects appear in new configurations? One attractive possibility suggested by theoretical models is that novelty detection relies upon a comparison between current sensory input and stored representations [3,4,5,6,7,8,9]
Activations shown on the averaged structural MRI scan of the 17 participants
Summary
We have all had the experience of walking into a familiar place, for example our living room, and immediately noticing that a new object such as a painting is present (i.e., stimulus novelty), or that the furniture has been rearranged (i.e., associative novelty). The hippocampus, is viewed to detect ‘‘associative mismatches’’ in the environment, i.e., when current sensory input conflicts with expectations deriving from associative retrieval of past experience [3,4,5,10,11,12]. By this account, we only notice that our favourite armchair has moved because we have expectations, derived from prior experience, about where it should be located
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