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Hippocampal brain-network coordination during volitional exploratory behavior enhances learning

Abstract

Exploratory behaviors during learning determine what is studied and when, helping to optimize subsequent memory performance. To elucidate the cognitive and neural determinants of exploratory behaviors, we manipulated the control that human subjects had over the position of a moving window through which they studied objects and their locations. Our behavioral, neuropsychological and neuroimaging data indicate that volitional control benefits memory performance and is linked to a brain network that is centered on the hippocampus. Increases in correlated activity between the hippocampus and other areas were associated with specific aspects of memory, which suggests that volitional control optimizes interactions among specialized neural systems through the hippocampus. Memory is therefore an active process that is intrinsically linked to behavior. Furthermore, brain structures that are typically seen as passive participants in memory encoding (for example, the hippocampus) are actually part of an active network that controls behavior dynamically as it unfolds.

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Figure 1: Volitional control enhances spatial and object-specific memory.
Figure 2: Volitional control confers no perceptual benefit.
Figure 3: Volitional control caused disproportionate memory enhancement with increasing study durations.
Figure 4: Volitional control does not benefit memory performance in amnesia subjects with hippocampal amnesia.
Figure 5: A coordinated brain network for volitional control.

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Acknowledgements

Research was supported by a US National Institutes of Health (NIH) Pathway to Independence award (K99-NS069788) and a Beckman Institute Postdoctoral Fellowship Award to J.L.V., by funds from the Kiwanis Foundation to D.T.T., and by NIH grants MH062500 to N.J.C. and NS19632 to D.T.T.

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Contributions

J.L.V., N.J.C., B.D.G. and K.D.F. conceived the experiments. J.L.V. designed and performed the experiments and analyzed data. D.T. provided access and support for testing subjects with amnesia. All authors co-wrote the paper, discussed results and commented on the manuscript.

Corresponding author

Correspondence to Joel L Voss.

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The authors declare no competing financial interests.

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Voss, J., Gonsalves, B., Federmeier, K. et al. Hippocampal brain-network coordination during volitional exploratory behavior enhances learning. Nat Neurosci 14, 115–120 (2011). https://doi.org/10.1038/nn.2693

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