Figure 2: Summary of known speed-related functional
anatomy
Effects of speed on either rate or temporal codes have been reported in
various interconnected brain regions that represent multiple, parallel,
functional ‘speed circuits’.
A: Circuits extracting speed information from motor input.
Speed signaling is extensive throughout the motor system, including in
motor cortex (Leinweber et al., 2017; von Nicolai et al., 2014),
striatum (see Fig. 1C), and the mesencephalic locomotor region (MLR)
(see Fig. 1B). The MLR projects to the basal forebrain, including the
medial septum/diagonal band of Broca (MSDB) (see Fig. 1), which itself
projects the hippocampal-entorhinal complex in a manner that could
logically produce a local motor-reflective speed signal (see Fig. 1).
During locomotion, MSDB also transmits efference copy-like signals to
various sensory cortices (Pinto et al., 2013; Fu et al., 2014; Lee et
al., 2014) that are themselves interconnected (Fu et al., 2014) and
contain various locomotive and/or speed signals (Fu et al., 2014; Pakan
et al., 2016; Roth et al., 2016; Erisken et al., 2014; Saleem et al.,
2013; Christensen and Pillow, 2017; Schneider et al., 2014; Chorev et
al., 2016). Motor cortical areas, specifically M2, also provides these
efference copies via direct innervation of the sensory areas (Schneider
et al., 2014; Leinweber et al., 2017). While diverse speed codes are
common throughout this circuitry, the only area that has only been
reported to contain a consistently diminished network effect with speed
and/or locomotion is auditory cortex (Schneider et al., 2014; Zhou et
al., 2014).
B: Circuits extracting speed information from sensory input.
Sensory information may also reach the hippocampal-entorhinal complex to
influence speed signaling via many putative circuits, at least one of
which has consistently reported speed effects. The retina projects to
the LGN and encodes information about optic flow speed. LGN cellular rates encode running speed (Roth et al., 2016;
Eriksen et al., 2014; but see Niell and Stryker,
2010), while this area serves as the primary source for visual
information in visual cortex (Niell 2015). Running speed and locomotion
more broadly seem to modulate processing in the visual cortex in a
variety of ways, particularly in V1 (Fu et al., 2014; Pakan et al.,
2016; Roth et al., 2016; Erisken et al., 2014; Saleem et al., 2013;
Christensen and Pillow, 2017). Visual cortex in turn projects to the
posterior parietal cortex (PPC) (Miller and Vogt, 1984), which has been
recently reported to also contain a temporal speed signal (Yang et al.,
2017). PPC next innervates the postrhinal cortex (PRC) (Burwell and
Amaral, 1998), which displays similar speed modulation (Furtak et al.,
2012). Finally, PRC innervates the hippocampal-entorhinal complex
(Burwell and Amaral, 1998; Agster and Burwell, 2009).
C: Circuits encoding speed that may also influence ongoing locomotion.
Recent evidence has suggested that the relationship between MSDB, and
possibly even hippocampal-entorhinal speed signaling and locomotive
speed may in fact be bidirectional as it is in areas such as the MLR
(Bender et al., 2015; Fuhrmann et al., 2015; Vandecasteele et al., 2014,
see Fig. 1). A few interconnected circuits have been hypothesized to
provide the anatomical underpinnings for this possibility (Fuhrmann et
al., 2015; Bender et al., 2015): MSDB projects directly to the ventral
tegmental area (VTA) (Fuhrmann et al., 2015; Geisler and Wise, 2008),
which in turn projects to various motor system areas, including motor
cortex and the striatum (Mogenson et al., 1980; Hosp et al., 2011;
Kunori et al., 2014; Beier et al., 2015). The hippocampal-entorhinal
system may be able to utilize the same circuit to influence the ongoing
locomotive state, through its projections to the lateral septum (LS) and
the following LS-to-lateral hypothalamus (LH) projections (Bender et
al., 2015; Geisler and Wise, 2008). Every area within these circuits
have been reported to contain speed signals of some type (Zhou et al.,
1999; Puryear et al., 2010; Wang and Tsien, 2011; Bender et al., 2015)
and to induce locomotive changes upon direct stimulation (Fuhrmann et
al., 2015; Kalivas et al., 1981; Parker and Sinnamon, 1983; Christopher
and Butter, 1968; Patterson et al., 2015; Bender et al., 2015).