TY - JOUR
T1 - Stimulation of the posterior cingulate cortex impairs episodic memory encoding
AU - Natu, Vaidehi S.
AU - Lin, Jui Jui
AU - Burks, Alexis
AU - Arora, Akshay
AU - Rugg, Michael D.
AU - Lega, Bradley
N1 - Funding Information:
Received Feb. 19, 2019; revised May 29, 2019; accepted July 10, 2019. Author contributions: V.S.N. and B.L. designed research; V.S.N., J.-J.L., A.B., A.A., and B.L. performed research; V.S.N. and J.-J.L. analyzed data; V.S.N. and B.L. wrote the paper; M.D.R. edited the paper. This work was funded by the National Institute of Neurological Disorders and Stroke–National Institutes of Health (Grant R01 NS107357-02 to B.L.). The authors declare no competing financial interests. Correspondence should be addressed to Vaidehi S. Natu at vaidehi.natu@utsouthwestern.edu.
Publisher Copyright:
Copyright © 2019 the authors.
PY - 2019/9/4
Y1 - 2019/9/4
N2 - Neuroimaging experiments implicate the posterior cingulate cortex (PCC) in episodic memory processing, making it a potential target for responsive neuromodulation strategies outside of the hippocampal network. However, causal evidence for the role that PCC plays in memory encoding is lacking. In human female and male participants (N = 17) undergoing seizure mapping, we investigated functional properties of the PCC using deep brain stimulation (DBS) and stereotactic electroencephalography. We used a verbal free recall paradigm in which the PCC was stimulated during presentation of half of the study lists, whereas no stimulation was applied during presentation of the remaining lists. We investigated whether stimulation affected memory and modulated hippocampal activity. Results revealed four main findings. First, stimulation during episodic memory encoding impaired subsequent free recall, predominantly for items presented early in the study lists. Second, PCC stimulation increased hippocampal gamma-band power. Third, stimulation-induced hippocampal gamma power predicted the magnitude of memory impairment. Fourth, functional connectivity between the hippocampus and PCC predicted the strength of the stimulation effect on memory. Our findings offer causal evidence implicating the PCC in episodic memory encoding. Importantly, the results indicate that stimulation targeted outside of the temporal lobe can modulate hippocampal activity and impact behavior. Furthermore, measures of connectivity between brain regions within a functional network can be informative in predicting behavioral effects of stimulation. Our findings have significant implications for developing therapies to treat memory disorders and cognitive impairment using DBS.
AB - Neuroimaging experiments implicate the posterior cingulate cortex (PCC) in episodic memory processing, making it a potential target for responsive neuromodulation strategies outside of the hippocampal network. However, causal evidence for the role that PCC plays in memory encoding is lacking. In human female and male participants (N = 17) undergoing seizure mapping, we investigated functional properties of the PCC using deep brain stimulation (DBS) and stereotactic electroencephalography. We used a verbal free recall paradigm in which the PCC was stimulated during presentation of half of the study lists, whereas no stimulation was applied during presentation of the remaining lists. We investigated whether stimulation affected memory and modulated hippocampal activity. Results revealed four main findings. First, stimulation during episodic memory encoding impaired subsequent free recall, predominantly for items presented early in the study lists. Second, PCC stimulation increased hippocampal gamma-band power. Third, stimulation-induced hippocampal gamma power predicted the magnitude of memory impairment. Fourth, functional connectivity between the hippocampus and PCC predicted the strength of the stimulation effect on memory. Our findings offer causal evidence implicating the PCC in episodic memory encoding. Importantly, the results indicate that stimulation targeted outside of the temporal lobe can modulate hippocampal activity and impact behavior. Furthermore, measures of connectivity between brain regions within a functional network can be informative in predicting behavioral effects of stimulation. Our findings have significant implications for developing therapies to treat memory disorders and cognitive impairment using DBS.
KW - Deep brain stimulation
KW - Episodic memory
KW - Functional connectivity
KW - Hippocampus
KW - Posterior cingulate cortex
KW - Stereotactic electroencephalography
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U2 - 10.1523/JNEUROSCI.0698-19.2019
DO - 10.1523/JNEUROSCI.0698-19.2019
M3 - Article
C2 - 31358651
AN - SCOPUS:85071786280
SN - 0270-6474
VL - 39
SP - 7173
EP - 7182
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 36
ER -