Precise control of theta frequency by acceleration during spatial navigation

EMILIO KROPFF; EDVARD MOSER; MAY-BRITT MOSER; ERIC CARMICHAEL

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

The theta rhythm organizes neural activity in the hippocampus and entorhinal cortex of rats, packing related information for the purpose of local network computations (Gupta et al., 2012; Mizuseki et al., 2009). An additional coding role for the theta cycle has been proposed, explaining the correlation between spiking position and theta phase found in spatial fields (O'Keefe and Recce 1993, Hafting, Fyhn et al. 2008) as a result of a strict linear dependence of theta frequency on running speed (Geisler, Robbe et al. 2007, Jeewajee, Barry et al. 2008). However, very little is known about the modulation of theta frequency by other navigational variables that might interfere with this proposed mechanism. By means of a recently introduced protocol that allows the disentanglement of kinematic variables, we here show that the theta band frequency of both local field potential oscillations and single cell rhythmic spiking is modulated by positive-only acceleration rather than speed. This non-linear relationship, confirmed in free foraging open-field experiments, makes the integral of theta frequency path-dependent (nonholonomic) and in consequence non-univocally related not only to displacement but also to any other kinematic variable. Our results suggest that variations in theta frequency rather reflect a precise mechanism for speeding up computations in the entorhinal-hippocampal circuits. This global mechanism, triggered by highly specific behaviors, could produce a greater number of computational epochs per second, thus reducing systematic errors in linear calculations of trajectory.