Summary & Future Directions
Here, we have reviewed the evidence for robust rate and temporal codes for speed throughout the mammalian brain. These codes are especially well-documented in the hippocampus and entorhinal cortex, where they likely play essential roles in the maintenance of stable spatial representations. Codes for speed exist in both upstream motor and sensory circuitry, and we argue that the work performed thus far suggests these different modalities interact in a complex way to ultimately give rise to the speed information processed by the hippocampal-entorhinal complex.
A number of unresolved issues preclude a more complete understanding of the neural speed signal. One such issue concerns the purpose of diverse rate codes. For example, in nearly every region reviewed here, positively- and negatively-speed modulated cells have been reported. Further investigation is required to determine whether these opposing codes work cohesively to produce a singular, robust internal measure of speed or if they might instead either conflict with each other or possibly encode distinct components of speed or velocity.
With respect to the origin of the unified speed hippocampal-entorhinal speed signal, both motor and sensory speed coding should be investigated simultaneously to parse out their relative relationships to each other (as in Campbell et al., 2018) and to downstream speed signaling. Speed estimates could be theoretically distilled by many sensory modalities, and yet speed signaling has only begun to be examined in full in the visual system. Why might the auditory system, for instance, receive an efference copy from M2 of an opposite polarity from that received by the visual system (Schneider et al., 2014; Leinweber et al., 2017; Zhou et al., 2014; Dadarlat and Stryker, 2017), and do these distinct polarities impact the relative contribution of either sense to the hippocampal-entorhinal speed signal?
Another sensory modality warranting serious consideration in the search for the speed signal origin is the vestibular system. Vestibular information has been suggested to be integrated with input from other senses such as vision as well as motor efference copy to produce a substantial portion of the sensation of self-motion (reviewed in Cullen, 2012). Additionally, vestibular input is utilized by head-direction cells for their processing, and may be influential in other elements of spatial cognition and navigation (Cullen, 2012). While at least one group has reported diminished entorhinal speed modulations in response to inactivation of the vestibular nuclei (Jacob et al., 2014), functional spatial processing and associated speed-based changes have been achieved in experiments utilizing virtual reality and head-fixation protocols (Domnisoru et al., 2013; Heys et al., 2014; Justus et al., 2017; Campbell et al., 2018; Heys and Dombeck, 2018), which presumably disrupt vestibular sensation. It has been suggested that the visual system may be able to compensate for missing vestibular contributions to speed signaling in these experimental conditions (Jacob et al., 2014), but this notion may be complicated by findings of altered speed signaling in vertically-locomoting animals who are also experiencing altered vestibular afferents (Casali et al., 2019).
The idea that speed signaling in noncanonically motor control regions such as MSDB (Fuhrmann et al., 2015; Bender et al., 2015; but see Bland et al., 2006) and possibly the hippocampus (Bender et al., 2015) can influence ongoing locomotive behavior also invites further discussion. How might these structures control descending locomotive outputs? A few of the groups reporting these effects (Fuhrmann et al., 2015; Bender et al., 2015) have proposed various circuits that may relay septo-hippocampal/entorhinal speed signaling to locomotive control regions, primarily ones converging upon the ventral tegmental area (VTA) (Fig. 2C). This putative functional anatomy includes a direct MSDB-to-VTA projection (Fuhrmann et al., 2015; Geisler and Wise, 2008) and a hippocampal-originating projection that goes through first the lateral septum and next the lateral hypothalamus before reaching the VTA (Bender et al., 2015; Geisler and Wise, 2008). All of these regions have been shown to contain rate codes for speed (Zhou et al., 1999; Puryear et al., 2010; Wang and Tsien, 2011; Bender et al., 2015) and to modulate locomotion upon stimulation (Kalivas et al., 1981; Parker and Sinnamon, 1983; Christopher and Butter, 1968; Patterson et al., 2015; Bender et al., 2015). Moreover, the VTA makes functional connections with the nucleus accumbens (NAc), striatum, and motor cortex (Mogenson et al., 1980; Hosp et al., 2011; Kunori et al., 2014; Beier et al., 2015), providing access to canonical locomotive control circuitry. Furthermore, glutamatergic projections seem to be a major component of these VTA-converging, locomotion-controlling pathways (Fuhrmann et al., 2015; Geisler and Wise, 2008). Despite the reviewed effects of MSDB glutamatergic stimulation on hippocampal-entorhinal speed encoding, recent investigation also suggests that these speed effects may be at least partially mediated by local glutamatergic projections onto other MSDB cell types projecting to the hippocampal-entorhinal complex (Fuhrmann et al., 2015; Robinson et al., 2016). These two lines of evidence suggest that the MSDB glutamatergic population may represent the segregators of the region’s speed signal’s distinct functions, sending speed-scaled output to locomotive circuitry while simultaneously transmitting an efference copy-like signal to the other MSDB cells to convey to the hippocampal-entorhinal complex for use in spatial representations and possible locomotive feedback.
Finally, while the contents of this review have for the most part intentionally avoided discussing any possible distinct encoding mechanisms for speed and acceleration, it should be noted that, while underreported relative to speed, acceleration-specific coding has indeed been reported (Kemere et al., 2013; Long et al., 2014). It has been further suggested that acceleration, and not speed, may in fact dominate aspects of temporal coding of movement (Long et al., 2014; Kropff Causa et al., unpublished), but further experimentation is required to support this notion.