A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning

By Michael E. Hasselmo, Clara Bodelón, B. Wyble. Neural Computation, 2002

896 citations recorded by the source corpus.

The theta rhythm appears in the rat hippocampal electroencephalogram during exploration and shows phase locking to stimulus acquisition. Lesions that block theta rhythm impair performance in tasks requiring reversalofpriorlearning, includingreversalinaT-maze, whereassociations between one arm location and food reward need to be extinguished in favor of associations between the opposite arm location and food reward. Here, a hippocampal model shows how theta rhythm could be important for reversal in this task by providing separate functional phases during each 100-300 msec cycle, consistent with physiological data. In the model, effective encoding of new associations occurs in the phase when synaptic input from entorhinal cortex is strong and long-term potentiation (LTP) of excitatory connections arising from hippocampal region CA3 is strong, but synaptic currents arising from region CA3 input are weak (to prevent interference from prior learned associations). Retrieval of old associations occurs in the phase when entorhinal input is weak and synaptic input from region CA3 is strong, but when depotentiation occurs at synapses from CA3 (to allow extinction of prior learned associations that do not match current input). These phasic changes require that LTP at synapses arising from region CA3 should be strongest at the phase when synaptic transmission at these synapses is weakest. Consistent with these requirements, our recent data show that synaptic transmission in stratum radiatum is weakest at the positive peak of local theta, which is when previous data show that induction of LTP is strongest in this layer.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/6e0737b49ad276d264fe17b5c8d561d3dfcdd081

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Citations in the corpus

What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data (2005, methodology): “…will briefly review four complementary and interacting hypotheses: (1) theta rhythm provides separation between encoding and retrieval dynamics (Hasselmo et al., 2002b), (2) theta rhythm enhances the context-dependent retrieval of previously encoded sequences (Hasselmo and Eichenbaum, 2005),…”
The role of phase synchronization in memory processes (2011, background): “Phase synchronization in the theta range may define instances when information transfer is likely to result in long-term memory formatio”
Complementary learning systems within the hippocampus: A neural network modeling approach to reconciling episodic memory with statistical learning (2016, methodology): “These phases have been proposed to correspond to encoding- and retrieval-like states: A strong influence of ECin on CA1 — a state where the external environment directly influences CA1 — is considered more akin to encoding, while a strong influence of CA3 on CA1 is more akin to retrieval (21).”
Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop (2009, background): “…hippocampus and EC do not have a fixed theta phase preference; their phase varies systematically as a function of behavior (O’Keefe and Recce, 1993; Hafting et al., 2008), pointing to a role of the local circuits in controlling place cell discharges (Tsodyks et al., 1996; Hasselmo et al., 2002).”
Temporal encoding of place sequences by hippocampal cell assemblies. (2006, background): “Several computational models and empirical observations are compatible with the above scenario (Hebb, 1949; Levy and Steward, 1979; Lisman and Idiart, 1995; Muller et al., 1996; Jensen and Lisman, 1996; Mehta et al., 1997; Wallenstein and Hasselmo, 1997; Samsonovich and McNaughton, 1997; Tsodyks, 19”
Reactivation of behavioral activity during sharp waves: A computational model for two stage hippocampal dynamics (2007, neutral): “5) (Hasselmo et al., 2002).”
Tracelink: A model of consolidation and amnesia (2005, positive): “The stability-plasticity dilemma has been addressed by relatively few researchers (Carpenter & Grossberg, 1988; Grossberg, 1976, 1987; Hasselmo, 1994; Hasselmo, Bodelon, & Wyble, 2002; Meeter, Talamini, & Murre, in press; Murre, 1992).”
Theta and Gamma Oscillations during Encoding Predict Subsequent Recall (2003, neutral): “During a working memory task, hippocampal theta appears phase locked to stimuli (Givens, 1996), providing a possible mechanism for sensory encoding (Hasselmo et al., 2002).”
Frontal midline EEG dynamics during working memory (2005, background): “Many theories of theta function in the hippocampus suggest that theta regulates timing of spike-mediated information transmission, specifically by behaviorally relevant phase precession of neuronal firing relative to theta phase (Bose et al., 2000; Buzsaki, 2002; Hasselmo et al., 2002; Yamaguchi, 20”
From modulated Hebbian plasticity to simple behavior learning through noise and weight saturation (2012, background): “Relearning and rememorization of an acquired behavior is an important property of animal behavior (Staddon, 1983), also called reversal (Hasselmo et al., 2002).”