Theta Rhythms & Running Speed
Two hippocampal oscillations exhibit prominent speed-based modulation: theta (roughly 6-12Hz) and gamma (roughly 25-100Hz). Theta oscillations are canonically associated with active behavioral states such as locomotion or REM sleep (Buzsáki 2002; 2005; Colgin 2013; Korotkova et al., 2018). The relationship between theta and running speed has been an active research topic for nearly half a century, beginning with Vanderwolf’s seminal finding that the locomotion speed of a rat roughly correlated with the strength of the hippocampal EEG theta signal (Vanderwolf 1969). This relationship was further outlined in the following years by studies specifically detailing enhancements of theta amplitude and frequency (Whishaw and Vanderwolf, 1973; McFarland et al., 1974; Arnolds et al., 1979) at high running speeds. Various contemporary studies have replicated both effects in mice and rats throughout the hippocampus (Shen et al., 1997; Rivas et al., 1996; Sławińska and Kasicki, 1998; Geisler et al., 2007; 2010; Bender et al., 2015; Gereke et al., 2017; Scaplen et al., 2017; Winne et al., 2019), and a recent report has provided confirmation of similar changes in temporal lobe theta in humans (Aghajan et al., 2017). Moreover, the waveform shape of theta oscillations also appears to shift at higher running speeds from a classic sinusoidal pattern to a sawtooth-like pattern (Buzsáki et al., 1983; Terrazas et al., 2005; Sheremet et al., 2016).
The correlation between hippocampal theta and running speed is most prominent in CA1: when speed modulation of theta was tracked in rats in CA1, CA3, and DG, frequency changes occurred in all three regions, but strong power changes were limited to CA1 (Montgomery et al., 2009; Hinman et al. 2011). Given that CA1 receives anatomically distinct inputs from those of CA3 and DG (Fig. 2) (Amaral and Witter, 1989; Witter and Amaral, 2004), it seems likely that the observed findings reflect differential delivery routes for the putative speed signal to each hippocampal area. Moreover, long axis effects on the CA1 temporal signal also seem to exist, with speed modulations of theta power and waveform shape appearing strongest in dorsal CA1 and diminishing in ventral CA1 (Maurer et al., 2005; Hinman et al., 2011; Patel et al., 2012; Hinman et al., 2013; Sheremet et al., 2016). Modulations of frequency remain constant along the long-axis of CA1 (Maurer et al., 2005; Hinman et al., 2011; Mikulovic et al., 2018; but see Sheremet et al., 2016), a division that might reflect the differential projections along the long axis and their proposed resultant functional gradients (Strange et al., 2014).
MEC exhibits similar theta oscillatory activity during locomotion to that observed in the hippocampus, and, reflecting communication between the two regions, theta-band coherence with the hippocampus (Buzsáki et al., 1986; Brankačk et al., 1993). Theta power and frequency in the MEC also both scale with running speed (Hinman et al., 2016; Jeewajee et al., 2008; Wills et al., 2012) (Fig. 2D), and thus, entorhinal-hippocampal theta-band coherence improves as a function of speed (Hinman et al., 2011). However, as MEC fails to display a CA1-like long axis effect on the speed-theta relationship, there subsequently exists a septotemporal drop-off in the speed-based inter-area theta coherence (Hinman et al., 2011).
While most of the literature covering the entorhinal speed signal describes modulations occurring specifically in MEC, it should be noted that speed effects on theta frequency and power have also been shown to occur in the lateral entorhinal cortex (LEC) (Hinman et al., 2011), despite being a markedly less spatially modulated region (Hargreaves et al., 2005). The LEC sends its own projections throughout the hippocampus (Witter and Amaral, 2004; Agster and Burwell, 2013), and recent work has accordingly demonstrated that inactivating the LEC with muscimol, a GABAergic agonist, results in a decrease in hippocampal CA1 theta power and frequency, and reduces the strength of hippocampal speed-theta correlations (Scaplen et al., 2017). Both the LEC and MEC have recently been implicated in temporal encoding (Heys and Dombeck, 2018; Tsao et al., 2018), a role that one would certainly expect to influence any downstream encoding of a variable defined with respect to time (e.g., speed). Thus, speed modulated theta-frequency inputs from both the MEC and LEC play a role in shaping speed and theta-dependent computations in the hippocampus itself.