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 (Berson class papers). LGN cellular rates encode running speed (Roth et al., 2016; Eriksen et al., 2014; Berson class papers?; 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).