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

Pierantonio Parmiani,Cristina Lucchetti,Gianfranco Franchi

doi:10.3389/fnbeh.2018.00024

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.

Highlights

Sensory-motor integration involves coupling the sensory system and motor system
To measure the time spent in locating the slot, in control rats we identified the video frame in which the longer mystacial macrovibrissae first contacted the front wall of the box (Figure 1A) and the first frame showing the nose inside the slot, and calculated the interval between
Previous studies have found a significant role of whisker sense in many types of motor behavior (Anjum et al, 2006; Hartmann, 2011; Grant et al, 2012), but its role in skilled reaching has never previously been explored

Summary

Introduction

Sensory-motor integration involves coupling the sensory system and motor system. It is not a static process, since for a given behavior there is no one single sensory input and no one single motor command. Multisensory integration allows information from the different sensory modalities, such as sight, sound, touch, taste, smell and self-motion, to guide motor behavior (Kleinfeld and Deschênes, 2011; Kleinfeld et al, 2014; Miller et al, 2017). A suitable model for studying multisensory integration in motor behavior is the so called ‘‘skilled reaching’’, a complex movement common to many animal species, in which a forelimb is extended to grasp food that is placed in the mouth for eating. Multiple parallel parietofrontal circuits, devoted to specific sensorimotor transformations during skilled reaching, have been described in monkeys (Matelli and Luppino, 2001; Omrani et al, 2016, 2017), and evidence from functional brain imaging studies suggests that the organization of this complex behavior is based on the same principles in humans (Sacrey et al, 2009; Filimon, 2010)

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