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Research Articles, Behavioral/Cognitive

Hippocampal and Prefrontal Theta-Band Mechanisms Underpin Implicit Spatial Context Learning

Eelke Spaak and Floris P. de Lange
Journal of Neuroscience 2 January 2020, 40 (1) 191-202; DOI: https://doi.org/10.1523/JNEUROSCI.1660-19.2019
Eelke Spaak
Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, 6525 EN, Nijmegen, The Netherlands
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Floris P. de Lange
Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, 6525 EN, Nijmegen, The Netherlands
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Abstract

Humans can rapidly and seemingly implicitly learn to predict typical locations of relevant items when those items are encountered in familiar spatial contexts. Two important questions remain, however, concerning this type of learning: (1) which neural structures and mechanisms are involved in acquiring and exploiting such contextual knowledge? (2) Is this type of learning truly implicit and unconscious? We now answer both these questions after closely examining behavior and recording neural activity using MEG while observers (male and female) were acquiring and exploiting statistical regularities. Computational modeling of behavioral data suggested that, after repeated exposures to a spatial context, participants' behavior was marked by an abrupt switch to an exploitation strategy of the learnt regularities. MEG recordings showed that hippocampus and prefrontal cortex (PFC) were involved in the task and furthermore revealed a striking dissociation: only the initial learning phase was associated with hippocampal theta band activity, while the subsequent exploitation phase showed a shift in theta band activity to the PFC. Intriguingly, the behavioral benefit of repeated exposures to certain scenes was inversely related to explicit awareness of such repeats, demonstrating the implicit nature of the expectations acquired. Together, these findings demonstrate that (1a) hippocampus and PFC play complementary roles in the implicit, unconscious learning and exploitation of spatial statistical regularities; (1b) these mechanisms are implemented in the theta frequency band; and (2) contextual knowledge can indeed be acquired unconsciously, and awareness of such knowledge can even interfere with the exploitation thereof.

SIGNIFICANCE STATEMENT Human visual perception is determined not just by the light that strikes our eyes, but also strongly by our prior knowledge and expectations. Such expectations, particularly about where to expect certain objects given scene context, might be learned implicitly and unconsciously, although this is hotly debated. Furthermore, it is unknown which brain mechanisms underpin this type of learning. We now show that, indeed, spatial prior expectations can be learned without awareness; in fact, strikingly, awareness seems to hinder the exploitation of the relevant knowledge. Furthermore, we demonstrate that one brain mechanism (hippocampal theta-band activity) is responsible for learning in these settings, whereas another mechanism (prefrontal theta-band activity) is involved in exploiting the learned associations.

  • contextual cueing
  • hippocampus
  • implicit learning
  • magnetoencephalography
  • theta rhythm
  • visual search
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The Journal of Neuroscience: 40 (1)
Journal of Neuroscience
Vol. 40, Issue 1
2 Jan 2020
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Hippocampal and Prefrontal Theta-Band Mechanisms Underpin Implicit Spatial Context Learning
Eelke Spaak, Floris P. de Lange
Journal of Neuroscience 2 January 2020, 40 (1) 191-202; DOI: 10.1523/JNEUROSCI.1660-19.2019

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Hippocampal and Prefrontal Theta-Band Mechanisms Underpin Implicit Spatial Context Learning
Eelke Spaak, Floris P. de Lange
Journal of Neuroscience 2 January 2020, 40 (1) 191-202; DOI: 10.1523/JNEUROSCI.1660-19.2019
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Keywords

  • contextual cueing
  • hippocampus
  • implicit learning
  • magnetoencephalography
  • theta rhythm
  • visual search

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