Kinematic fields of the visuo-hippocampal circuit

The structure of focused receptive fields in retinotopic and allocentric space in the visual cortex and hippocampus is studied extensively to understand cognitive functions such as stimulus tracking and path-integration, respectively. These functions require accurate tracking of running speed and acceleration. While speed dependence in these areas is well-studied, acceleration-dependence has received little attention, and the joint effect of speed-acceleration is unknown. Hence, we assessed the joint influence of these kinematic variables by computing receptive fields in a novel, 2D, phase space of speed-acceleration using the Allen Brain Visual Observatory data. Head-fixed mice ran spontaneously on a running wheel next to a monocular gray screen ensuring virtually no changes in the retinotopic or allocentric space. Remarkably, about half (44.3%, 6590/14862) of neurons in the visuo-hippocampal circuit (from LGN to subiculum) were significantly modulated by a specific combination of speed and acceleration to form receptive fields in the speed-acceleration phase space (called kinematic space). The prevalence of kinematic tuning is comparable to the fraction of place cells in the mouse hippocampus, and the fraction of visually tuned neurons in higher visual areas. The kinematic field size (~30% of the sampled space) was also comparable to the place field size. Kinematic fields spanned the entire space but preferred either low-speed, high-acceleration or the high-speed, low-acceleration segments. Although pupil size too varied spontaneously, the kinematic tuning exceeded pupil size tuning in all brain areas. Surprisingly, pupil size modulated the activity of ~20% of hippocampal neurons, which was comparable to that in LGN and visual cortical areas. Thus, all visuo-hippocampal areas have focused kinematic fields that are three times more prevalent than the pupil size fields in the absence of any vestibular, visual or spatial stimuli. This kinematic phase space could interface with retinotopic and allocentric spaces to guide natural behaviors involving movement.