Whisker and Nose Tactile Sense Guide Rat Behavior in a Skilled Reaching Task

Abstract

Skilled reaching is a complex movement in which a forelimb is extended to grasp food for eating. Video-recordings analysis of control rats enables us to distinguish several components of skilled reaching: Orient, approaching the front wall of the reaching box and poking the nose into the slot to locate the food pellet; Transport, advancing the forelimb through the slot to reach-grasp the pellet; and Withdrawal of the grasped food to eat. Although food location and skilled reaching is guided by olfaction, the importance of whisker/nose tactile sense in rats suggests that this too could play a role in reaching behavior. To test this hypothesis, we studied skilled reaching in rats trained in a single-pellet reaching task before and after bilateral whisker trimming and bilateral infraorbital nerve (ION) severing. During the task, bilaterally trimmed rats showed impaired Orient with respect to controls. Specifically, they detected the presence of the wall by hitting it with their nose (rather than their whiskers), and then located the slot through repetitive nose touches. The number of nose touches preceding poking was significantly higher in comparison to controls. On the other hand, macrovibrissae trimming resulted in no change in reaching/grasping or withdrawal components of skilled reaching. Bilaterally ION-severed rats, displayed a marked change in the structure of their skilled reaching. With respect to controls, in ION-severed rats: (a) approaches to the front wall were significantly reduced at 3–5 and 6–8 days; (b) nose pokes were significantly reduced at 3–5 days, and the slot was only located after many repetitive nose touches; (c) the reaching-grasping-retracting movement never appeared at 3–5 days; (d) explorative paw movements, equal to zero in controls, reached significance at 9–11 days; and (e) the restored reaching-grasping-retracting sequence was globally slower than in controls, but the success rate was the same. These findings strongly indicate that whisker trimming affected Orient, but not the reaching-grasping movement, while ION severing impaired both Orient (persistently) and reaching-grasping-retracting (transiently, for 1–2 weeks) components of skilled reaching in rats.

A kinematic study of skilled reaching movement in rat

“…Videotaped movements were analysed frame-by-frame using Avidemux 2.6 software (www.avidemux. org) (Parmiani et al, 2018).…”

“…1, frames A1-E1 on the right). The task began when the rat walked from the back to the front wall of the box with a cyclical motion of the limbs, a head-down posture and exploratory whisking, until the whiskers came into contact with the front wall (Parmiani et al, 2018). Immediately after the whiskers touched the front wall (˜20 ms, unpublished data), the orienting movement began with the approach of the head to the front wall and ended at the start of reaching, with the nose poking through the slot to sniff the pellet (Fig.…”

“…Skilled reaching, the act of reaching to grasp an object as occurs in a reach-to-eat task, shares many similarities among both primates and rodents (Whishaw and Pellis, 1990;Whishaw, 1996). In rodents, skilled reaching to eat is a learned and composite movement in which the rat, inside a reaching box, uses olfactory cues, proprioception, whiskers, and tactile nose sense to locate food, and to define a reaching path for the paw to target the pellet (Whishaw and Tomie, 1989;Whishaw et al, 2017;Parmiani et al, 2018). Skilled reaching task starts with orienting, which consists of the rat's approach to the front wall of the reaching box, and nose positioning over the pellet.…”

“…The rat's skilled reaching behaviour emerges as an important model for investigating many topics in neurosciences research, from motor behaviour (Whishaw and Tomie, 1989;Alaverdashvili et al, 2008) to sensorimotor integration (Whishaw and Pellis, 1990;Hermer-Vazquez et al, 2007;Parmiani et al, 2018), or to study neural mechanisms of movement (Azim et al, 2014) and also serves as a model for studying many motor system injuries that affect motor behaviour (Klein et al, 2012;Viaro et al, 2017).…”

“…Skilled reaching has been previously described in rats by means of notation techniques (Whishaw et al, 1992;Gharbawie and Whishaw, 2006), video , as well as cineradiographic recordings (Alaverdashvili et al, 2008). More recently, high-speed single (Wong et al, 2015;Ellens et al, 2016;Nica et al, 2018;Parmiani et al, 2018) and multiple cameras have respectively been used in kinematic studies to reconstruct reaching trajectories (Azim et al, 2014;Mathis et al, 2018;Bova et al, 2019). The most recent innovation for describing/analysing rat reaching, how ever, includes a machine-learning algorithm to enable digitization of joint segments from markerless video recordings (Mathis et al, 2018;Bova et al, 2019).…”