Theta Rhythm Across the Species: Bridging Inconsistencies With a Multiple Memory Systems Approach Shanny Foo and Veronique D. Bohbot Douglas Mental Health University Institute, Department of Psychiatry, Faculty of Medicine, McGill University The discovery of movement-modulated 7– 8 Hz theta rhythm in rodents provided one of the earliest indications of synchronicity of neuronal firing in the hippocampus. Subsequent research expanded on this finding on theta rhythm and its role in other domains such as spatial navigation and memory. Never- theless, discrepancies among animal models posed the question of how well the animal literature represents human mechanisms. Technological advances have since facilitated research taking place directly in humans, typically neurosurgical patients implanted with intracranial electrodes. Human studies have observed lower frequency oscillations in participants engaged in virtual spatial navigation studies, compared to the 7– 8 Hz oscillations seen in rodents. Recently, research in humans engaged in real-world task demonstrating 7–9 Hz oscillations infer that the previously observed lower frequency theta may have been constrained by the absence of movement-related processing that occurs in physical activities. Together, these findings suggest that humans may indeed be more similar to rodent models than previously reported when completing tasks more analogous to those used in rodent experiments. This review summarizes early work on theta rhythm across species and outlines certain remaining discrepancies as well as a novel proposed hypothesis of the behavioral correlates of theta rhythm, taking a multiple memory systems perspective. Keywords: theta rhythm, hippocampus, caudate nucleus, spatial navigation, memory The theta rhythm is a neural oscillatory pattern, typically in the 6 –9 Hz range, and has been associated with synaptic activity in the hippocampus (Buzsáki et al., 2012), a multimodal structure anatom- ically connected to cortical areas throughout the brain, particularly in regions important for episodic (Tulving, 1972) and spatial (O’Keefe & Nadel, 1978) memory. First discovered in the 1950s, low frequency oscillations in the 5–7 Hz range were observed during arousal in rabbits, when they were alert and showing interest in environmental surroundings (Green & Arduini, 1954). Oscillations in the 6 –9 Hz also seem to be movement-related as prominent changes specific to the hippocampus in this frequency band have been detected in rodents during movement initiation (Vanderwolf, 1969) and in proportion to changes in magnitude (Czurko et al., 1999; Vanderwolf, 1969; Whishaw & Vanderwolf, 1973) and speed (McFarland et al., 1975). Examination of movement during spatial navigation has yielded in- sights into the specific aspects of spatial memory that modulate theta rhythm (Huxter et al., 2003; Mehta et al., 2002; Moser et al., 2008; O’Keefe & Dostrovsky, 1971; Olvera-Cortés et al., 2002; Skaggs et al., 1996). Nevertheless, the relationship between theta rhythm, move- ment, and spatial navigation is unclear, as animal models have pro- vided diverse results in the 4 –12 Hz frequency band. For instance, aside for the 6 –9 Hz previously discussed in rats, 7–9 Hz theta activity has been recorded in mice and cats, whereas 4 –7 Hz activity has been observed in dogs (Bender et al., 2015; Black & Young, 1972; G. Buzsáki, 2002; Kemp & Kaada, 1975; Vanderwolf, 1969). On the other hand, research conducted on nonhuman primates during active movement exhibited an absence of theta rhythm (Talakoub et al., 2019), as have studies in bats, which have also demonstrated an absence of theta rhythm, alluding to possible alternate mechanisms (Barry & Doeller, 2013; Giocomo & Moser, 2011; Yartsev et al., 2011). These oscillations, at approximately 1.5 Hz, infer that bats indeed have oscillatory patterns associated with navigation and move- ment, but at lower frequency bands (Heys et al., 2013; Yartsev et al., 2011). Nevertheless, it is possible that the low firing rate and short recording time of bat neurons may obscure detection of theta rhyth- micity (Barry, Bush, et al., 2012). On the whole, the intriguing divergence in findings among animal models underlines the necessity of additional research investigating other potential factors implicated in the modulation of theta rhythm. More recent research has provided some clarity on the question of how animal models may translate to humans while providing additional clues into the broader relationship between theta rhythm and other cognitive domains ( Aghajan et al., 2017; Bohbot et al., 2017; Caplan et al., 2003; Clemens et al., 2013; de Araújo et al., 2002; Ekstrom et al., 2005; Goyal et al., 2020; Guitart-Masip et al., 2013; Halgren, 1991; Jun et al., 2020; Lega et al., 2012; Ravassard et al., 2013; Staudigl & Hanslmayr, 2013; Watrous et al., 2011). For instance, Bohbot et al. (2017) compared real-world navigation tasks to virtual navigation tasks in humans, reveal- Shanny Foo X https://orcid.org/0000-0002-8544-8319 Veronique D. Bohbot X https://orcid.org/0000-0003-3738-2770 Shanny Foo is now at the Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University. Shanny Foo served as lead for writing (original draft). Veronique D. Bohbot served as lead for conceptualization, funding acquisition, and supervision. Shanny Foo and Veronique D. Bohbot contributed to writing (review and editing) equally. Correspondence concerning this article should be addressed to Veronique D. Bohbot, Douglas Mental Health University Institute, Department of Psy- chiatry, Faculty of Medicine, McGill University, FBC Building, 6875 Boule- vard LaSalle, Verdun, QC H4H 1R3, Canada. Email: veronique.bohbot@ mcgill.ca This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly. Behavioral Neuroscience © 2020 American Psychological Association 2020, Vol. 134, No. 6, 475– 490 ISSN: 0735-7044 https://doi.org/10.1037/bne0000440 475