Rhythmic coordination of hippocampal neurons during associative memory processing

Abstract

Hippocampal oscillations are dynamic, with unique oscillatory frequencies present during different behavioral states. To examine the extent to which these oscillations reflect neuron engagement in distinct local circuit processes that are important for memory, we recorded single cell and local field potential activity from the CA1 region of the hippocampus as rats performed a context-guided odor-reward association task. We found that theta (4–12 Hz), beta (15–35 Hz), low gamma (35–55 Hz), and high gamma (65–90 Hz) frequencies exhibited dynamic amplitude profiles as rats sampled odor cues. Interneurons and principal cells exhibited unique engagement in each of the four rhythmic circuits in a manner that related to successful performance of the task. Moreover, principal cells coherent to each rhythm differentially represented task dimensions. These results demonstrate that distinct processing states arise from the engagement of rhythmically identifiable circuits, which have unique roles in organizing task-relevant processing in the hippocampus.DOI: http://dx.doi.org/10.7554/eLife.09849.001

Defining the synaptic mechanisms that tune CA3-CA1 reactivation during sharp-wave ripples

“…In our study, we consider spikes of pyramidal cells to represent information content and spikes of inhibitory cells to contribute to the shape of overall network dynamics (ending a sharp wave in CA3, and pacing the frequency of ripples in CA1). This idea is consistent with experimental data which has found a heightened specificity in the activation of hippocampal pyramidal cells compared to hippocampal interneurons across the various rhythmic activities which mark different phases in information processing in an in vivo task (Rangel et al 2016).…”

High-order theta harmonics account for the detection of slow gamma

“…In particular, wavelet and EEMD 480 yielded results congruent with the idea of "low gamma" while under representing the harmonics 481 of theta (which exist in the raw trace as a sawtooth shape; Buzsáki et al, 1985;Sheremet et al, 482 2016). This phenomenon occurs to an extreme in the dentate gyrus, which exhibits up to the 5 th 483 harmonic of theta, spilling into the range that has been defined recently as beta (Rangel et al,484 2015; Rangel et al, 2016) or potentially slow gamma . 485…”

Multiple modes of hippocampal–prefrontal interactions in memory-guided behavior

“…In addition to these three network patterns, other oscillations have also been proposed to play a role in governing hippocampal-prefrontal interactions, including beta oscillations [16,20], and 4 Hz rhythms [62]. Hence, converging lines of evidence indicate a highly dynamic, multiple-scale organization comprised of network patterns that can engage coordination between the hippocampus and prefrontal cortex.…”

“…In order to understand the influence of separate physiological patterns on cognition, examining a diverse array of behavior tasks will be necessary [4,20,23,26,27,30,56]. Investigating interactions during the learning and performance stages of complex tasks that manifest distinctive cognitive demands, such as encoding, retrieval, novelty, and flexibility, can reveal the specific network pattern(s) that are prevalent during these periods.…”

“…However, current evidence remains primarily phenomenological, and a causal demonstration that coherence of network rhythms plays a specific role in cognitive processing is still lacking. Multiple network patterns have been ascribed roles in organizing local processing in the hippocampal network during behavior, including slow theta oscillations (6–12 Hz), beta (15–20 Hz) and gamma rhythms (40–100 Hz), and fast network oscillations, in particular sharp-wave ripples (SWRs, 150–250 Hz) [7,13,18–20]. Similarly, multiple rhythms are also implicated in information processing in PFC [11,14,21–24].…”