Toward a Physiologic Explanation of Behavioral Data on Human Memory: The Role of Theta-Gamma Oscillations and NMDAR-Dependent LTP

Lisman, John; Jensen, Ole; Kahana, Michael J.

doi:10.1017/cbo9780511529818.010

Cited by 4 publications

(3 citation statements)

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“…These studies led to remarkable discoveries regarding the role of theta oscillations and place cell activity in animal learning (see J. Lisman, Jensen, & Kahana, 2001, for a review). While human scalp EEG studies had suggested some role for theta rhythms in cognitive processes (e.g., Schacter, 1977) it was only at the turn of the 21st century that depth-electrode recordings in neurosurgical patients specifically implicated theta oscillations in human spatial and verbal memory (Kahana, Sekuler, Caplan, Kirschen, & Madsen, 1999; Sederberg, Kahana, Howard, Donner, & Madsen, 2003; Ekstrom et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…Whereas lesion studies reified the single-case study of H.M. (Squire, Knowlton, & Musen, 1993), further advances in our understanding of hippocampal physiology arose from recording field potentials and neuronal spiking in awake behaving mammals (e.g., O’Keefe & Dostrovsky, 1971; Knierim, Kudrimoti, & McNaughton, 1995; McNaughton, Barnes, & O’Keefe, 1983). These studies led to discoveries regarding the role of theta oscillations and place cell activity in animal learning (see J. Lisman, Jensen, & Kahana, 2001, for a review).…”

Section: Introductionmentioning

confidence: 99%

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Hippocampal theta and episodic memory

Rudoler

Herweg

Kahana

2022

Preprint

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Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsaki & Moser, 2013; J.E. Lisman & Jensen, 2013), yet human hippocampal recordings have shown divergent theta correlates of memory formation. Herweg et al. (2020) suggest that decreases in memory-related broadband power mask narrowband theta increases. Their survey also suggests that theta's role in memory appears strongest in contrasts that isolate associative retrieval processes and when aggregating signals across large brain regions. We evaluate these hypotheses by analyzing human hippocampal recordings captured as 161 neurosurgical patients performed a free recall task. Using the irregular-resampling auto-spectral analysis to separate broad and narrow-band components of the field potential we show: 1) Broadband and narrowband components of theta exhibit opposite effects, with broadband signals decreasing and narrow-band theta increasing during successful encoding; 2) Whereas low-frequency theta oscillations increase prior to successful recall, higher-frequency theta and alpha oscillations decrease, masking theta's positive effect when aggregating across the full band; 3) Theta's effects on memory encoding and retrieval do not differ between reference schemes that accentuate local signals (bipolar) and those that aggregate across large reference (whole brain average). In line with computational models that ascribe a fundamental role for hippocampal theta in memory our large-scale study of human hippocampal recordings shows that 3-4 Hz theta oscillations reliably increase during successful memory encoding and prior to spontaneous recall of previously studied items.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Hippocampal theta and episodic memory

Rudoler

Herweg

Kahana

2022

Preprint

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“…3Biologically inspired nonlinear networks can also perform autoassociation and heteroassociation (e.g., Chappell & Humphreys, 1994; Lisman, Jensen, & Kahana, 2001). We analyze linear DMMs because analytic expressions for their behavior can be easily obtained (Weber, 1988).…”

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confidence: 99%

Theoretical Correlations and Measured Correlations: Relating Recognition and Recall in Four Distributed Memory Models.

Kahana¹,

Rizzuto²,

Schneider³

2005

Journal of Experimental Psychology: Learning, Memory, and Cogni

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This article addresses the relation between item recognition and associative (cued) recall. Going beyond measures of performance on each task, the analysis focuses on the degree to which the contingency between successful recognition and successful recall of a studied item reflects the commonality of memory processes underlying the recognition and recall tasks. Specifically, 4 classes of distributed memory models are assessed for their ability to account for the relatively invariant correlation (approximately .5) between successive recognition and recall. Basic versions of each model either under- or overpredict the intertask correlation. Introducing variability in goodness-of-encoding and response criteria, as well as output encoding, enabled all 4 models to reproduce the moderate intertask correlation and the increase in correlation observed in 2 mixed-list experiments. This model-based analysis provides a general theoretical framework for interpreting contingencies between successive memory tests.

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Hippocampal Theta and Episodic Memory

2022

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Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsáki and Moser, 2013; Lisman and Jensen, 2013), yet human hippocampal recordings have shown divergent theta correlates of memory formation. Herweg et al. (2020) suggest that decreases in memory-related broadband power mask narrowband theta increases. Their survey also notes that the theta oscillations appear most prominently in contrasts that isolate memory retrieval processes and when aggregating signals across large brain regions. We evaluate these hypotheses by analyzing human hippocampal recordings captured as 162 neurosurgical patients (n= 86 female) performed a free recall task. Using the Irregular-Resampling Auto-Spectral Analysis (IRASA) to separate broad and narrowband components of the field potential, we show that (1) broadband and narrowband components of theta exhibit opposite effects, with broadband signals decreasing and narrowband theta increasing during successful encoding; (2) whereas low-frequency theta oscillations increase before successful recall, higher-frequency theta and alpha oscillations decrease, masking the positive effect of theta when aggregating across the full band; and (3) the effects of theta on memory encoding and retrieval do not differ between reference schemes that accentuate local signals (bipolar) and those that aggregate signals globally (whole-brain average). In line with computational models that ascribe a fundamental role for hippocampal theta in memory, our large-scale study of human hippocampal recordings shows that 3–4 Hz theta oscillations reliably increase during successful memory encoding and before spontaneous recall of previously studied items.SIGNIFICANCE STATEMENTAnalyzing recordings from 162 participants, we resolve a long-standing question regarding the role of hippocampal theta oscillations in the formation and retrieval of episodic memories. We show that broadband spectral changes confound estimates of narrowband theta activity, thereby accounting for inconsistent results in the literature. After accounting for broadband effects, we find that increased theta activity marks successful encoding and retrieval of episodic memories, supporting rodent models that ascribe a key role for hippocampal theta in memory function.

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Toward a Physiologic Explanation of Behavioral Data on Human Memory: The Role of Theta-Gamma Oscillations and NMDAR-Dependent LTP

Cited by 4 publications

References 0 publications

Hippocampal theta and episodic memory

Hippocampal theta and episodic memory

Theoretical Correlations and Measured Correlations: Relating Recognition and Recall in Four Distributed Memory Models.

Hippocampal Theta and Episodic Memory

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