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Scientific Understanding of Consciousness |
Associative Memory and Cortical-Hippocampal Brain Networks
Science 29 August 2014: Vol. 345 no. 6200 pp. 1054-1057 Targeted enhancement of cortical-hippocampal brain networks and associative memory Jane X. Wang, et.al. 1Department of Medical Social Sciences, Ken and Ruth Davee Department of Neurology, and Interdepartmental Neuroscience Program, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA. 2The Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, IL, USA. 3Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA. [paraphrase] The influential notion that the hippocampus supports associative memory by interacting with functionally distinct and distributed brain regions has not been directly tested in humans. We therefore used targeted noninvasive electromagnetic stimulation to modulate human cortical-hippocampal networks and tested effects of this manipulation on memory. Multiple-session stimulation increased functional connectivity among distributed cortical-hippocampal network regions and concomitantly improved associative memory performance. These alterations involved localized long-term plasticity because increases were highly selective to the targeted brain regions, and enhancements of connectivity and associative memory persisted for ~24 hours after stimulation. Targeted cortical-hippocampal networks can thus be enhanced noninvasively, demonstrating their role in associative memory. The hippocampus is necessary for associative (relational/declarative) memory. It is a neuroanatomical convergence zone for highly processed sensory information regarding qualities of objects and contexts and therefore could serve as a “hub” to support binding of information from distinct processing modules into associative memories. However, hippocampal interactivity with distributed brain regions has yet to be demonstrated as necessary for associative memory in humans. Few experiments have used functional magnetic resonance imaging (fMRI) to identify hippocampal interactions with distributed cortical regions that are correlated with associative memory. Although brain-lesion studies have shown the necessity of an intact hippocampus for associative memory, they cannot readily demonstrate the necessity of hippocampal interactivity with other regions. We therefore developed methods to modulate cortical-hippocampal brain networks in healthy adults (n = 16 subjects) in order to test their role in associative memory. We focused modulatory stimulation on the lateral parietal cortex component of a well-characterized cortical-hippocampal network on the basis of hypothesized interactions between hippocampus and lateral parietal cortex in memory as well as robust functional connectivity between these regions, which is likely mediated by lateral parietal projections to retrosplenial and parahippocampal cortex. We defined a target within the left hippocampus for each subject and used resting-state fMRI to identify a subject-specific left lateral parietal location that demonstrated high functional connectivity with the hippocampal target. Noninvasive high-frequency repetitive transcranial magnetic stimulation (rTMS) was delivered to the parietal location for 5 consecutive days on the basis of evidence that rTMS can induce changes in connectivity within stimulated networks and that such effects can increase over multiple-day stimulation sessions. These findings confirm the proposed role of cortical-hippocampal interactions in associative memory. Enhanced memory via neurosurgical (invasive) stimulation of entorhinal cortex (the primary input to hippocampus) has been reported, although effects were specific to the material studied during stimulation, and network-level function was not tested. Our findings thus demonstrate persistent memory changes and substantiate fMRI correlative evidence for cortical-hippocampal network involvement in associative memory. These findings confirm the proposed role of cortical-hippocampal interactions in associative memory. Enhanced memory via neurosurgical (invasive) stimulation of entorhinal cortex (the primary input to hippocampus) has been reported, although effects were specific to the material studied during stimulation, and network-level function was not tested. Our findings thus demonstrate persistent memory changes and substantiate fMRI correlative evidence for cortical-hippocampal network involvement in associative memory.
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