Stimulation of the Posterior Cingulate Cortex Impairs Episodic Memory Encoding.

J Neurosci 2019 09 29;39(36):7173-7182. Epub 2019 Jul 29.

Department of Neurological Surgery, University of Texas Southwestern Medical Center, Dallas, Texas 75390, and.

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 ( = 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. Cognitive impairment and memory loss are critical public health challenges. Deep brain stimulation (DBS) is a promising tool for developing strategies to ameliorate memory disorders by targeting brain regions involved in mnemonic processing. Using DBS, our study sheds light on the lesser-known role of the posterior cingulate cortex (PCC) in memory encoding. Stimulating the PCC during encoding impairs subsequent recall memory. The degree of impairment is predicted by stimulation-induced hippocampal gamma oscillations and functional connectivity between PCC and hippocampus. Our findings provide the first causal evidence implicating PCC in memory encoding and highlight the PCC as a favorable target for neuromodulation strategies using connectivity measures to predict stimulation effects. This has significant implications for developing therapies for memory diseases.

Download full-text PDF

Source
http://dx.doi.org/10.1523/JNEUROSCI.0698-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6733540PMC
September 2019

Publication Analysis

Top Keywords

memory encoding
24
episodic memory
16
memory
15
pcc
12
cingulate cortex
12
posterior cingulate
12
causal evidence
12
stimulation
11
hippocampal activity
8
stimulation memory
8
stimulation dbs
8
deep brain
8
brain stimulation
8
stimulation-induced hippocampal
8
free recall
8
study lists
8
evidence implicating
8
memory disorders
8
cognitive impairment
8
pcc memory
8

Altmetric Statistics

Similar Publications

The effect of hippocampal function, volume and connectivity on posterior cingulate cortex functioning during episodic memory fMRI in mild cognitive impairment.

Eur Radiol 2017 Sep 13;27(9):3716-3724. Epub 2017 Mar 13.

Alzheimer Center, Department of Neurology, VU University Medical Center, Neuroscience Campus, Amsterdam, The Netherlands.

Objectives: Diminished function of the posterior cingulate cortex (PCC) is a typical finding in early Alzheimer's disease (AD). It is hypothesized that in early stage AD, PCC functioning relates to or reflects hippocampal dysfunction or atrophy. The aim of this study was to examine the relationship between hippocampus function, volume and structural connectivity, and PCC activation during an episodic memory task-related fMRI study in mild cognitive impairment (MCI). Read More

View Article and Full-Text PDF
September 2017

Modulation of Oscillatory Power and Connectivity in the Human Posterior Cingulate Cortex Supports the Encoding and Retrieval of Episodic Memories.

J Cogn Neurosci 2017 Aug 7;29(8):1415-1432. Epub 2017 Apr 7.

University of Texas at Dallas.

Existing data from noninvasive studies have led researchers to posit that the posterior cingulate cortex (PCC) supports mnemonic processes: It exhibits degeneration in memory disorders, and fMRI investigations have demonstrated memory-related activation principally during the retrieval of memory items. Despite these data, the role of the PCC in episodic memory has received only limited treatment using the spatial and temporal precision of intracranial EEG, with previous analyses focused on item retrieval. Using data gathered from 21 human participants who underwent stereo-EEG for seizure localization, we characterized oscillatory patterns in the PCC during the encoding and retrieval of episodic memories. Read More

View Article and Full-Text PDF
August 2017

A functional magnetic resonance imaging study mapping the episodic memory encoding network in temporal lobe epilepsy.

Brain 2013 Jun 14;136(Pt 6):1868-88. Epub 2013 May 14.

Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.

Functional magnetic resonance imaging has demonstrated reorganization of memory encoding networks within the temporal lobe in temporal lobe epilepsy, but little is known of the extra-temporal networks in these patients. We investigated the temporal and extra-temporal reorganization of memory encoding networks in refractory temporal lobe epilepsy and the neural correlates of successful subsequent memory formation. We studied 44 patients with unilateral temporal lobe epilepsy and hippocampal sclerosis (24 left) and 26 healthy control subjects. Read More

View Article and Full-Text PDF
June 2013

Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans.

Hippocampus 2017 10 30;27(10):1040-1053. Epub 2017 Jun 30.

Department of Neurological Surgery, University of Texas, Southwestern Medical Center, Dallas, Texas, 75390.

Functional differences in the anterior and posterior hippocampus during episodic memory processing have not been examined in human electrophysiological data. This is in spite of strong evidence for such differences in rodent data, including greater place cell specificity in the dorsal hippocampus, greater sensitivity to the aversive or motivational content of memories in ventral regions, connectivity analyses identifying preferential ventral hippocampal connections with the amygdala, and gene expression analyses identifying a dorsal-ventral gradient. We asked if memory-related oscillatory patterns observed in human hippocampal recordings, including the gamma band and slow-theta (2. Read More

View Article and Full-Text PDF
October 2017