Rhythms of the hippocampal network

Abstract

The hippocampal local field potential (LFP) exhibits three major types of rhythms, theta, sharp wave-ripples and gamma. These rhythms are defined by their frequencies, have behavioral correlates in several species including rats and humans, and have been proposed to perform distinct functions in hippocampal memory processing. However, recent findings have challenged traditional views on these behavioral functions. Here I review our current understanding of the origins and mnemonic functions of hippocampal theta, sharp-wave ripples and gamma rhythms based on findings from rodent studies, and present an updated, synthesized view of their roles and interactions within the hippocampal network.

Spatial representation in the hippocampal formation: a history

“…In shying away from the memory functions of the hippocampus, we shall also pass over the vast and growing literature on how replay and preplay of firing sequences may enable consolidation and storage of hippocampal memory through interactions with neocortical neural networks [51][52][53][54] , and we shall not discuss the important but separate question of whether or how place cells are used for goal-directed navigation and route planning [55][56][57][58][59] . We have also left out dozens of pioneering studies of temporal coding and network oscillations, including theta rhythms, that have shaped our current understanding of hippocampal function beyond the representation of space 49,[60][61][62] . Finally, this review is dominated by work in rats and mice, reflecting the use of freely moving rodents as subjects in nearly all studies of spatially modulated cells in the hippocampal formation (see Box 1 for extensions to the primate brain).…”

Mechanisms underlying memory enhancement in humans

“…Slow gamma is thought to be driven by CA3 (Belluscio, Mizuseki, Schmidt, Kempter, & Buzsaki, 2012;Colgin et al, 2009;Kemere, Carr, Karlsson, & Frank, 2013;Schomburg et al, 2014) and couples activity in hippocampal sub-region CA1 to inputs from CA3. Memories are thought to be stored in and retrieved from the CA3 network (Brun et al, 2002;Nakazawa et al, 2002;Steffenach, Sloviter, Moser, & Moser, 2002;Treves & Rolls, 1992), thus a plausible hypothesis is that slow gamma promotes memory retrieval as suggested in (Colgin, 2016). By contras fast gamma is thought to be entrained by inputs from MEC (Belluscio et al, 2012;Colgin et al, 2009;Kemere et al, 2013;Schomburg et al, 2014) which in turn is thought to process sensory information and transmit this information to the hippocampus (Canto, Wouterlood, & Witter, 2008).…”

“…However, there is more recent evidence that theta can be intrinsically being generated within the hippocampal structure CA3 (Buzsáki, 2002;Kocsis, Bragin, & Buzsáki, 1999;Konopacki, Bland, & Roth, 1987) and CA1 (Goutagny, Jackson, & Williams, 2009). This theta rhythm has been functionally related with learning and memory, synaptic plasticity, coordination of neuronal activity, active sampling of sensory stimuli, among others (reviewed in Colgin, 2016). Interestingly, in human hippocampus this theta rhythm is thought to be less prominent -smaller in amplitude and duration-and typically identified at lower frequencies (Jacobs, 2013;Watrous, Lee, Izadi, & Gurkoff, 2013;Zhang & Jacobs, 2015).…”

“…By contras fast gamma is thought to be entrained by inputs from MEC (Belluscio et al, 2012;Colgin et al, 2009;Kemere et al, 2013;Schomburg et al, 2014) which in turn is thought to process sensory information and transmit this information to the hippocampus (Canto, Wouterlood, & Witter, 2008). Therefore, one plausible function for fast gamma is the encoding of current sensory information in memory (Colgin, 2016).…”

“…Hippocampal theta activity has been related to many aspects of cognition (Colgin, 2016), including memory and spatial navigation (Landfield, McGaugh, & Tusa, 1972;Seager, Johnson, Chabot, Asaka, & Berry, 2002;Winson & Abzug, 1978). Theta has been also shown to increase amplitude during hippocampal dependent behaviors (Vanderwolf, 1969), to modulate synaptic plasticity (Huerta & Lisman, 1995;Larson et al, 1986;Pavlides et al, 1988) and to coordinate neural networks (Buzsáki, 1996;Miller, 2013;Siapas, Lubenov, & Wilson, 2005;Sirota et al, 2008).…”