A Knowledge-Based Arrangement of Prototypical Neural Representation Prior to Experience Contributes to Selectivity in Upcoming Knowledge Acquisition

Hiroki Kurashige, Yuichi Yamashita, Takashi Hanakawa, Manabu Honda

Knowledge acquisition is a process in which one actively selects a piece of information from the environment and assimilates it with prior knowledge. However, little is known about the neural mechanism underlying selectivity in knowledge acquisition. Here we executed a 2-day human experiment to investigate the involvement of characteristic spontaneous activity resembling a so-called "preplay" in selectivity in sentence comprehension, an instance of knowledge acquisition. On day 1, we presented 10 sentences (prior sentences) that were difficult to understand on their own. On the following day, we first measured the resting-state functional magnetic resonance imaging (fMRI). Then, we administered a sentence comprehension task using 20 new sentences (posterior sentences). The posterior sentences were also difficult to understand on their own, but some could be associated with prior sentences to facilitate their understanding. Next, we measured the posterior sentence-induced fMRI to identify the neural representation. From the resting-state fMRI, we extracted the appearances of activity patterns similar to the neural representations for posterior sentences. Importantly, the resting-state fMRI was measured before giving the posterior sentences, and thus such appearances could be considered as preplay-like or prototypical neural representations. We compared the intensities of such appearances with the understanding of posterior sentences. This gave a positive correlation between these two variables, but only if posterior sentences were associated with prior sentences. Additional analysis showed the contribution of the entorhinal cortex, rather than the hippocampus, to the correlation. The present study suggests that prior knowledge-based arrangement of neural activity before an experience contributes to the active selection of information to be learned. Such arrangement prior to an experience resembles preplay activity observed in the rodent brain. In terms of knowledge acquisition, the present study leads to a new view of the brain (or more precisely of the brain's knowledge) as an autopoietic system in which the brain (or knowledge) selects what it should learn by itself, arranges preplay-like activity as a position for the new information in advance, and actively reorganizes itself.