Olfaction and whisker tactile sense in skilled reaching: behaviour and kinematics

1.1-Bulbectomy experiments We focused on how the rat uses olfactory cues in a single-pellet reaching task, which is composed of three sequential learned responses: Orient, Transport and Withdrawal. High-speed video-recording enabled us to describe the features of responses in controls vs. 3–5 and 12–14 days after bilateral bulbectomy in trials with (P trial) vs. without (no-P trial) pellet. In controls: a- the sequence of responses was complete in P trials, while it was interrupted after Orient in no P-trials; b- there is no difference in duration between the first two events of orient in P vs. no-P trials. After bulbectomy: a- the frequency of approach to the front wall decreased; b- the sequence of responses was complete in both P and no-P trials; c- there is an increase in Orient duration due solely to the increased time in slot localisation; d- the first nose contact with the front wall took place below the shelf/pellet level; e- the number of nose touches preceding poking was significantly higher. Otherwise, after Bulbectomy the pattern of reach and the ability to grasp the pellet do not change, suggesting that the preserved whisker/nose tactile input triggers the transport movement. In conclusion, bulbectomy, but not necessarily olfaction, affects Orienting whereas olfaction is used to navigate the box and determines the choice to reach/grasp the target. 1.2 - Bilateral Macrovibrissae trimming and Infraorbital nerve severing experiments Skilled reaching is a complex movement, in which a forelimb is extended to grasp food that is placed in the mouth for eating. In rat, olfaction is used to guide reaching, but the relevance of whisker sense suggests that this could also have a role. To test this hypothesis, we studied skilled reaching behaviour in rats trained in a single-pellet reaching task before and after infraorbital nerve (ION) severing. Bilaterally ION severed rats display an impressive change in the architecture of skilled behaviour already detectable in the first post-surgical recording session. Specifically, the behavioural sequence was interrupted either before approaching the front wall of the box or before poking with the nose into the slot to locate the food pellet. In the following days, rats began to display a new phase of exploration of the front wall with repetitive forelimb movements, a prelude to the reappearance of reaching, which took place between 6 and 12 days after ION severing, depending on the rat. From this time onward the skilled behaviour architecture completely recovered. These findings strongly indicate that whisker sense play a role in guiding skilled reaching behaviour in the rat. 1.3- Skilled Reaching Kinematics experiments In rats, skilled reaching includes orienting (OR), reaching (RC), grasping (GR) and retracting (RT) movements. Here we present the first quantitative description of this behaviour by means of a 3D recording system. OR movement featured three steps: head approaching the front wall (HA), slot localization with head movements (SL), and nose poke through it (PK). SL was the longest-lasting step (p=0.0000), while HA was the fastest (p=0.0000). RC showed two bimodal start point distributions: i) along the X axis, beyond or within the first quartile from the target, long and short RC trajectories were distinguished, each presenting different shapes and velocity peaks; ii) along the Z axis, there were two modalities of reach start, in the stance or swing phase of the last step. 3D plots evidenced that at the end of RC, the wrist/paw occupied the same spatial position as the nose at the end of OR. In GR, averaging the trajectories confirmed the lowering and approach of the marker towards the target. Averaging the velocity profile showed equal amplitude velocity peaks, at around 20–30% of the normalized GR duration, on the X and Z axes. Finally, logistic regression analysis suggested which kinematic variables were decisive for successful prehension.