Hippocampal theta rhythm: A tag for short‐term memory

Abstract

The theta rhythm is the largest extracellular synchronous signal that can be recorded from the mammalian brain, and has been strongly implicated in mnemonic functions of the hippocampus. We advance the proposal that the theta rhythm represents a "tag" for short-term memory processing in the hippocampus. We propose that the hippocampus receives two main types of input, theta from ascending brainstem-diencephalo-septal systems and "information bearing" mainly from thalamocortical and cortical systems. The temporal convergence of activity of these two systems results in the encoding of information in the hippocampus, primarily reaching it via cortical routes. By analogy to processes associated with long-term potentiation (LTP), we suggest that theta represents a strong depolarizing influence on NMDA receptor-containing cells of the hippocampus. The temporal coupling of a theta-induced depolarization and the release of glutamate to these cells from intra- and extrahippocampal sources activates them. This, in turn, initiates processes leading to a (short-term) strengthening of connections between presynaptic ("information bearing") and postsynaptic neurons of the hippocampus. Theta is selectively present in the rat during active exploratory movements. During exploration, a rat continually gathers and updates information about its environment. If this information is temporally coupled to theta (as with the case of locomotion), it becomes temporarily stored in the hippocampus by mechanisms similar to the early phase of LTP (E-LTP). If the exploratory behavior of the rat goes unreinforced, these relatively short-lasting traces (1-3 h) gradually weaken and eventually fade-to be reupdated. On the other hand, if the explorations of the rat lead to rewards (or punishments), additional modulatory inputs to the hippocampus become activated and convert the short-term, theta-dependent memory, into long-term stores.

A distinctive subpopulation of medial septal slow-firing neurons promote hippocampal activation and theta oscillations

“…In behaving animals, the short-lasting increase of theta power caused by the firing of these neurons may serve as short-term tags (Vertes 2005) and a favorable network state for synaptic plasticity (Larson et al 1986;Pavlides et al 1988). The consequent release of ACh in the hippocampus may, in parallel, act on muscarinic receptors to produce relatively long-lasting effects on promoting signaling pathways that lead to activation of kinases (Giovannini et al 2005) and immediate-early genes (Wirtshafter 2005).…”

Local Generation of Theta-Frequency EEG Activity in the Parasubiculum

“…The theta rhythm is a large-amplitude, sinusoidal EEG rhythm (4 -12 Hz) that is observed in entorhinal cortex, dentate gyrus, CA1, and CA3 regions of the hippocampal formation (Bland and Oddie 2001;Buzsaki 2002;Buzsaki et al 1983;Green and Arduini 1954;Petsche et al 1962). It has been linked to computational processes that mediate sensorimotor integration, spatial navigation, and memory formation (Bland 1986;Buzsaki 2005;Hasselmo 2005;Vertes 2005). The entorhinal cortex and the hippocampus express robust theta activity that is generated by network and cellular mechanisms including cholinergic and GABAergic inputs from the medial septum, rhythmic inhibitory inputs from local interneurons, and oscillations in membrane potential dependent on intrinsic voltage-dependent conductances (Alonso and Garcia-Austt 1987a,b;Buzsaki 2002;Chapman and Lacaille 1999a,b;Gloveli et al 2001Gloveli et al , 2005Klink and Alonso 1993;Leung and Yim 1991;Mitchell and Ranck 1980;Sotty et al 2003).…”

Exploratory Whisking by Rat Is Not Phase Locked to the Hippocampal Theta Rhythm

“…The importance of this issue is that locking can increase the reliability of synaptic transmission. This may provide a natural and efficient means to link the acquisition of new sen-sory information, such as that gleaned from vibrissa touch, with memories of past experiences and locations, whose storage and recall is dependent on hippocampal activity (Treves and Rolls, 1994;Buzsaki, 2002;Hasselmo, 2005;Vertes, 2005).…”