Abstract
Primary sensory neurons form the interface between world and brain. Their function is well-understood during passive stimulation but, under natural behaving conditions, sense organs are under active, motor control. In an attempt to predict primary neuron firing under natural conditions of sensorimotor integration, we recorded from primary mechanosensory neurons of awake, head-fixed mice as they explored a pole with their whiskers, and simultaneously measured both whisker motion and forces with high-speed videography. Using Generalised Linear Models, we found that primary neuron responses were poorly predicted by whisker angle, but well-predicted by rotational forces acting on the whisker: both during touch and free-air whisker motion. These results are in apparent contrast to previous studies of passive stimulation, but could be reconciled by differences in the kinematics-force relationship between active and passive conditions. Thus, simple statistical models can predict rich neural activity elicited by natural, exploratory behaviour involving active movement of sense organs.
Highlights
A major challenge of sensory neuroscience is to understand the encoding properties of neurons to the point that their spiking activity can be predicted in the awake animal, during natural behaviour
Our aim here was to predict spikes fired by primary whisker neurons (PWNs) of awake mice engaged in natural, object exploration behaviour
We assessed prediction performance using the other half of the data as a testing set: we provided the Generalised Linear Models (GLMs) with the whisker angle time series as input and calculated the predicted spike train, evoked in response (Materials and methods)
Summary
A major challenge of sensory neuroscience is to understand the encoding properties of neurons to the point that their spiking activity can be predicted in the awake animal, during natural behaviour. The videos were used to calculate the forces acting on the whiskers, and computational models were used to relate the activity of the neurons to the forces This approach allowed Campagner et al to predict the responses of the whisker neurons, even when the mice were exploring the pole freely and unpredictably, from knowledge of the forces that were acting on the whiskers. Together, these findings move the field of neuroscience forward by showing that sensory signals and neuronal responses can be correlated even in an awake animal. Our results provide a mechanical basis for linking receptor mechanisms to tactile behaviour
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