A brainstem/basal forebrain/cortical circuit for the neuronal coding of locomotion speed

NOUK TANKE; MIGUEL CARVALHO; MENNO WITTER; MAY-BRITT MOSER; EMILIO KROPFF; EDVARD MOSER

Congreso; 2017 Annual Meeting of the Society for Neurosciences; 2017

Speed cells in the medial entorhinal cortex (MEC) form a functionally distinct group of cells whose firing rate show either a positive or a negative linear correlation with locomotion speed. However, the origin of the speed signal in MEC is currently poorly understood. Previous studies have shown that stimulation of the pedunculopontine tegmental nucleus (PPN), a functional component of the brainstem?s mesencephalic locomotor region (MLR), is known to induce locomotion. Moreover, speed cells have been reported in this area; but it remains unclear whether and how signals from these neurons reach MEC. In this study, we investigated the possible implication of PPN for speed coding in MEC. Simultaneous anterograde and retrograde tracer injections, respectively in PPN and MEC, showed an indirect connection between these two areas, with a strong overlap between labelled PPN axons and MEC-projecting cell bodies in the basal forebrain, specifically the ventral medial septum and diagonal band of Broca (MS/DB). Chronic in vivo tetrode recordings during free foraging in an open field confirmed the presence of speed cells, with either a positive or a negative linear speed-rate relationship along this putative PPN-MS/DB-MEC circuit. In all three brain areas, positive speed cells showed prospective firing properties, consistent with the hypothesis that this speed signal may derive from a motor efferent copy in the brainstem. Conversely, the firing rate of negative speed cells correlates more closely to past speed. Optogenetic stimulation of channelrhodopsin-2-expressing neurons in PPN was followed, at regular latencies, by activation of a wide range of cells in both MS/DB and MEC, including speed cells, implicating the PPN as an upstream modulator of speed cell firing in both MS/DB and MEC. Together, our results suggest the presence of a functional connection between PPN, MS/DB and MEC for speed coding in the brain, with a possible relevance for higher order spatial mapping and navigation.