Elsevier

NeuroImage

Volume 114, 1 July 2015, Pages 257-263
NeuroImage

Decreases in theta and increases in high frequency activity underlie associative memory encoding

https://doi.org/10.1016/j.neuroimage.2015.03.077Get rights and content

Highlights

  • Intracranial encephalography (iEEG) was used to explore associative memory encoding.

  • Decreases in cortical low frequency activity are linked with associative encoding.

  • A progression of cortical high frequency activity increases mark encoding.

Abstract

Episodic memory encoding refers to the cognitive process by which items and their associated contexts are stored in memory. To investigate changes directly attributed to the formation of explicit associations, we examined oscillatory power captured through intracranial electroencephalography (iEEG) as 27 neurosurgical patients receiving subdural and depth electrodes for seizure monitoring participated in a paired associates memory task. We examined low (3–8 Hz) and high (45–95 Hz) frequency activity, and found that the successful formation of new associations was accompanied by broad decreases in low frequency activity and a posterior to anterior progression of increases in high frequency activity in the left hemisphere. These data suggest that the observed patterns of activity may reflect the neural mechanisms underlying the formation of novel item-item associations.

Introduction

When searching our memory for previously experienced episodes, we rely on retrieval cues established during memory encoding to target the desired memory. These retrieval cues can be shaped by environmental context, internal mental states, or by associations formed between items or events. For example, one may associate a given restaurant with an important conversation with a colleague; subsequent visits to the same restaurant may easily prompt recollection of that same conversation. Several theories of memory encoding posit computational correlates underlying the formation of such associations (Norman and O'Reilly, 2003, McClelland et al., 1995), and associative memory encoding appears to occupy a specific type of processing in the human memory system (Kahana, 2012). Functional MRI studies provide empiric evidence for the anatomic locations where these processes take place. These studies implicate the hippocampus and the perirhinal cortex in binding conceptual representations across distal and closely interacting cortical regions, respectively (Davachi et al., 2003, Mayes et al., 2007, Dalton et al., 2013). Despite theoretical and experimental work, however, understanding the specific neural mechanisms that underlie how associative memory encoding is mediated by the brain still remains an unresolved question.

Direct intracranial recordings during paired associates memory tasks offer an experimental paradigm well suited to directly explore this issue (Caplan, 2005). Participants in paired associates tasks are instructed to form explicit associations between items and then attempt to recall one member of each pair when the other is provided as a cue. Combining paired associates tasks with subsequent memory effect (SME) analyses, in which neural activity is compared between successful and unsuccessful encoding (Paller and Wagner, 2002, Sederberg et al., 2003), can isolate the neural mechanisms responsible for forming associations (Caplan and Glaholt, 2007, Molle et al., 2002). Intracranial electroencephalography (iEEG) recordings offer a range of benefits when compared to fMRI in investigating the precise spatiotemporal changes underlying this process (Jacobs and Kahana, 2010), but SME analyses using human iEEG have not been previously performed during a paired associates task.

We address this here by investigating the changes in neural activity underlying the successful formation of explicit associations using iEEG recordings captured from subdural and depth electrodes as 27 patients with medically refractory epilepsy participated in a paired associates memory task. Previous studies investigating changes in episodic memory related changes in iEEG activity have linked successful encoding with both increases and decreases in oscillatory power in multiple frequency bands (Nyhus and Curran, 2010). Most episodic memory tasks require encoding of both items and associations, however, and it is unclear whether these discrepancies may be related to the cognitive demands specific to the encoding task (Hanslmayr and Staudigl, 2013). Here, we directly compared changes in low (3–8 Hz; theta) and high (45–95 Hz; high gamma) frequency oscillatory power during the successful and unsuccessful encoding of explicit associations in order to investigate the neural mechanisms that specifically underlie associative memory encoding.

Section snippets

Materials and methods

Twenty seven participants with medication-resistant epilepsy underwent a surgical procedure in which platinum recording contacts were implanted subdurally on the cortical surface, as well as deep within the brain parenchyma. In each case, the clinical team determined the placement of the contacts so as to best localize epileptogenic regions. Data were collected at three different facilities: Hospital of the University of Pennsylvania (UP; Philadelphia, PA), Thomas Jefferson University Hospital

Results

Twenty seven participants with medication-resistant epilepsy who underwent a surgical procedure for placement of intracranial electrodes for seizure monitoring participated in a paired associates episodic verbal memory task during their hospital stay (Fig. 1a). Participants studied 235 ± 42 (mean ± SEM) word pairs. Participants successfully recalled 40.5% ± 5.7% words. On 9.8% ± 1.9% of trials, participants responded with intra-list intrusions (ILI). Participants responded with prior-list intrusions

Discussion

In order to directly examine the neural correlates of associative memory formation, we investigated iEEG spectral power during successful encoding as 27 participants performed a paired associates task. We examined LFA (3–8 Hz, theta) and HFA (45–95 Hz) and found that successful encoding was accompanied by broad decreases in LFA and corresponding increases in HFA. We found these changes most concentrated in the left temporal and frontal lobes and in the visual and MTL regions, although we also

Funding

This work was supported by the National Institutes of Health Intramural Research Program and by NIH grants MH055687, MH061975, NS067316, and MH017168.

Acknowledgments

We thank Dale H. Wyeth and Edmund Wyeth for technical assistance at Thomas Jefferson Hospital. The authors declare no competing financial interests. We are indebted to all patients who have selflessly volunteered their time to participate in our study.

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