Layer-Specific GABAergic Control of Distinct Gamma Oscillations in the CA1 Hippocampus

Abstract

The temporary interaction of distinct gamma oscillators effects binding, association, and information routing. How independent gamma oscillations are generated and maintained by pyramidal cells and interneurons within a cortical circuit remains unknown. We recorded the spike timing of identified parvalbumin-expressing basket cells in the CA1 hippocampus of anesthetized rats and simultaneously detected layer-specific gamma oscillations using current-source-density analysis. Spike timing of basket cells tuned the phase and amplitude of gamma oscillations generated around stratum pyramidale, where basket cells selectively innervate pyramidal cells with GABAergic synapses. Basket cells did not contribute to gamma oscillations generated at the apical tuft of pyramidal cells. This gamma oscillation was selectively modulated by a subset of local GABAergic interneurons and by medial entorhinal cortex layer 3 neurons. The generation of independent and layer-specific gamma oscillations, implemented onto hippocampal pyramidal cells along their somato-dendritic axis, can be explained by selective axonal targeting and precisely controlled temporal firing of GABAergic interneurons.

Intrinsic Cornu Ammonis Area 1 Theta-Nested Gamma Oscillations Induced by Optogenetic Theta Frequency Stimulation

“…We provide further evidence for an intrinsic CA1 gamma generator here by demonstrating that optogenetic theta stimulation of the CA1 causes a single gamma oscillation of a narrow frequency range that is independent of activity in the afferent regions. This in vitro CA1 gamma has several similarities with CA1 gamma in vivo, including a relatively fast frequency (Belluscio et al, 2012), similar phase-locking of CA1 gamma to the concurrent theta oscillation (Schomburg et al, 2014) and a similar phase delay between pyramidal neuron firing and interneuron firing within each gamma cycle (Senior et al, 2008;Lasztó czi and Klausberger, 2014). The presence of the alternating sinksource pair within the CA1 shows that the current generator is within the CA1 itself, as reflected by the reversal of the LFP between the SP and SLM.…”

Fear Memory

“…Thus there are "heterogeneous microcircuits between pyramidal and basket cells, which contributes to the sparse and distributed structure of hippocampal network activity" (339). The layer-specific interaction between pyramidal and basket cells underlies properties of the hippocampus, such as gamma oscillations, relevant to its physiology (334).…”

Inhibitory microcircuit modules in hippocampal learning

“…These studies have focused on hippocampal network activity patterns such as theta oscillations related to spatial navigation [41 ,42], gamma oscillations related to information binding and transmission [43 ], and SWR related to compressed replay of neuronal sequences during quiet wakefulness and slow-wave sleep [44]. A so-called hippocampal chronocycle has been suggested to orchestrate alternate functions of encoding and retrieval [45] through segregation at the ascending and peak phase of theta (acquisition) and at the descending and trough of theta (retrieval) [42,44].…”

“…A study from Klausberger and colleagues investigated how inhibition to distinct pyramidal neuron compartments relates to gamma oscillations in CA1 [43 ]. Two distinct gamma activities were generated near the soma and at distal dendritic tufts.…”