Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance

Abstract

The hippocampal formation is believed to be critical for the encoding, consolidation, and retrieval of episodic memories. Yet, how these processes are supported by the anatomically diverse hippocampal networks is still unknown. To examine this issue, we tested rats in a hippocampus-dependent delayed spatial alternation task on a modified T maze while simultaneously recording local field potentials from dendritic and somatic layers of the dentate gyrus, CA3, and CA1 regions by using high-density, 96-site silicon probes. Both the power and coherence of gamma oscillations exhibited layer-specific changes during task performance. Peak increases in the gamma power and coherence were found in the CA3-CA1 interface on the maze segment approaching the T junction, independent of motor aspects of task performance. These results show that hippocampal networks can be dynamically coupled by gamma oscillations according to specific behavioral demands. Based on these findings, we propose that gamma oscillations may serve as a physiological mechanism by which CA3 output can coordinate CA1 activity to support retrieval of hippocampusdependent memories.hippocampus ͉ local field potential ͉ retrieval ͉ synchrony B ased primarily on lesion studies, a consensus has emerged that the hippocampal formation is critical for episodic memories (1-3). In accord with lesion studies, the firing patterns of hippocampal and entorhinal neurons exhibit prospective and retrospective coding of episodic information (4-7). However, the specific roles of the various hippocampal subregions (8) responsible for encoding, consolidation, and retrieval of memory traces have been long debated. Computational models (9-12) have postulated the autoassociative recurrent network of the CA3 region as a suitable substrate for storing memories, which could be subsequently recalled via replay from CA3 to CA1. Circumscribed lesions in animals (13, 14) and genetic manipulations (15) also support the view that the integrity of the CA3 region is crucial in memory retrieval, but little is known about the physiological mechanisms of CA3-CA1 coordination that might support this process.Although recordings from multiple single neurons can assess the output representations of a network, the currently available large-scale unit recording methods do not have the ability to effectively monitor how information transfer is coordinated across several neuronal networks (16). On the other hand, although local field potentials (LFPs) lack single-neuron resolution, they reflect the temporal synchrony of local afferent activity and can effectively detect the changing modes of operation in local circuits (17)(18)(19). For example, synchronization of neuronal activity into coherent gamma-frequency oscillations can serve to bind representations (20, 21) and couple hippocampal and rhinal cortices during successful formation of declarative memories (22). To examine how regional networks within the hippocampal formation are dynamically coordinated during the retrieval process, we recorded LFP...

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“…Other corroborating observations come from the increased c-FOS activity in the hippocampus of B6 mice, which was largest for the drug that also induced the largest increase in gamma activity; that is YKP10A. Gamma activity in the hippocampus is thought to coordinate CA3 and CA1 networks during memory task performance (Montgomery and Buzsaki, 2007) in which c-FOS reactivity was exclusively found.…”

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

“…9,11,29 Moreover, the precise timing of action potentials is central for use-dependent synaptic plasticity and, thus, supports learning and memory formation. 13,20,30,31 In neuronal networks in vivo, gamma oscillations occur transiently on the hundred millisecond time scale upon sensory input or during specific cognitive tasks. In the human brain and dependent on the task, however, they can last for prolonged times in the range of minutes.…”

“…16,41 They can occur in the presence or in the absence of theta oscillations, 40,41 similar to the pattern of gamma oscillations in vivo. 8,30,48 Alternative models are based on the induction of transient phases of gamma oscillations: local tetanic electrical stimulation, topic application of potassium-rich solution, or application of metabotropic glutamate receptor agonists. 16,38,49 However, electrical stimulation of neuronal tissue can only partially mimic the features of naturally occurring network oscillations.…”

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

“…More recently, cortical inhibitory networks have also been proposed to play a critical role in the generation of faster activities that include oscillations in the low (i.e, beta-gamma oscillations at 20-80 Hz) and high frequency range (>80 Hz, so called ripples) (Buzsáki et al, 1992). Interestingly, both beta-gamma rhythms and ripples occurring in cortical areas (Gray et al, 1989;Murthy and Fetz, 1992;Singer and Gray, 1995), including those of the limbic system Chrobak and Buzsáki, 1998;Csicsvari et al, 1999Csicsvari et al, , 2003, have been implicated in higher brain processes such as attention, sensorimotor integration, consciousness, learning and memory (Girardeau et al, 2009;Montgomery and Buzsáki, 2007). Therefore, it has been suggested that these oscillatory rhythms represent the basic neuronal processing state of the brain (Basar et al, 1999).…”