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.