Bidirectional changes to hippocampal theta–gamma comodulation predict memory for recent spatial episodes

Abstract

Episodic memory requires the hippocampus, which is thought to bind cortical inputs into conjunctive codes. Local field potentials (LFPs) reflect dendritic and synaptic oscillations whose temporal structure may coordinate cellular mechanisms of plasticity and memory. We now report that single-trial spatial memory performance in rats was predicted by the power comodulation of theta (4-10 Hz) and low gamma (30-50 Hz) rhythms in the hippocampus. Theta-gamma comodulation (TGC) was prominent during successful memory retrieval but was weak when memory failed or was unavailable during spatial exploration in sample trials. Muscimol infusion into medial septum reduced the probability of TGC and successful memory retrieval. In contrast, patterned electrical stimulation of the fimbria-fornix increased TGC in amnestic animals and partially rescued memory performance in the water maze. The results suggest that TGC accompanies memory retrieval in the hippocampus and that patterned brain stimulation may inform therapeutic strategies for cognitive disorders.hippocampus | medial septum | theta-burst stimulation | fimbria-fornix | retrieval E pisodic memory stores the spatial, temporal, and personal contexts of events and requires the brain to represent temporally extended, sequential information (1). Cross-frequency power comodulation (2), defined as correlated spectral power fluctuations between different frequency waves (3), may provide a mechanism for coding episodic sequences by coordinating neuronal activity in timescales required for synaptic plasticity, memory encoding, and retrieval (4-6). A prominent theory suggests that ordered items in memory are coded by subdividing each hippocampal theta cycle (4-10 Hz) with multiple cortical gamma cycles . This temporal formatting may organize episodic sequences as coordinated firing of multiple cell assemblies (7-9). The theta-gamma discrete phase code hypothesis has been implemented in computational models (7), and neocortical thetagamma phase-amplitude correlation is observed in waking rats (10), accompanies working memory in humans (11), and recently has been linked to learning item-context associations in rats (12). Although phase-amplitude relations have been studied, less is known about correlations between theta and gamma power in the processes of memory acquisition and retrieval. Correlated theta and gamma power may be necessary for hippocampus-dependent memory, but this prediction has not been tested directly.Hippocampal theta and gamma oscillations have been associated independently with memory performance in many tasks. Theta rhythm correlates positively with learning in classical conditioning (13) and human episodic memory tasks (14, 15). Medial septal (MS) lesions reduce hippocampal theta rhythm and impair spatial memory in rats (16), as do infusions of muscimol (a GABA A agonist) into the MS (17, 18). Memory retrieval also has been associated with transient gamma oscillations in CA1 and CA3 (19). In particular, low gamma (30-50 Hz) activity may help couple CA3 and CA1...

Within-session dynamics of theta–gamma coupling and high-frequency oscillations during spatial alternation in rat hippocampal area CA1

“…In the rat hippocampus, there is a remarkable low-frequency activity, the well-known ''theta rhythm.'' It has been reported that the theta rhythm modulates gamma oscillations (Bragin et al 1995a;Tort et al 2008;Colgin et al 2009;Belluscio et al 2012) and their CFC alters depending on the running speed (Chen et al 2011;Ahmed and Mehta 2012) and the behavioral performance (Tort et al 2009;Shirvalkar et al 2010). Here we particularly focused on the CFC during a delay period, which several studies have suggested to require the involvement of hippocampus for successful task performance (Ainge et al 2007;Pastalkova et al 2008;Takahashi et al 2009a, b;MacDonald et al 2011).…”

Quantifying phase–amplitude coupling in neuronal network oscillations

“…This could allow for the simultaneous implementation of multiple coding schemes for memory items, stored in both a sequential and nonsequential context (Senior et al, 2008). Recent data from LFP recordings from both rat and human hippocampus provide evidence for a functional role of thetaegamma PAC in mnemonic processing (Axmacher et al, 2010;Shirvalkar et al, 2010;Tort et al, 2009), but these hippocampal models and examples also reflect a broader hypothesis of PAC function: hierarchies of inter-locked oscillatory frequencies allow ensembles of anatomically localized neurons co-active on short timescales (i.e. within higher-frequency cycles, e.g.…”

Transforms and Calculations: Behind the Mathematics of Psychophysiology

“…Researchers have employed amplitude-phase comodulation as well as phase-phase comodulation. The form commonly referenced in EEG literature is amplitude-amplitude power comodulation and is generally reported as a correlation coefficient (Shirvalkar, Rapp, & Shapiro, 2010). Collura (2008) noted the similarity between the equation for comodulation and Pearson's correlation while pointing out that the comodulation measurements are ''amplitudes across time.''…”