California sea lions employ task-specific strategies for active touch sensing

ABSTRACT Active sensing is the process of moving sensors to extract task-specific information. Whisker touch is often referred to as an active sensory system as whiskers are moved with purposeful control. Even though whisker movements are found in many species, it is unknown whether any animal can make task-specific movements with their whiskers. California sea lions (Zalophus californianus) make large, purposeful whisker movements and are capable of performing many whisker-related discrimination tasks. Therefore, California sea lions are an ideal species to explore the active nature of whisker touch sensing. Here, we show that California sea lions can make task-specific whisker movements. California sea lions move their whiskers with large amplitudes around object edges to judge size, make smaller, lateral stroking movements to judge texture and make very small whisker movements during a visual task. These findings, combined with the ease of training mammals and measuring whisker movements, makes whiskers an ideal system for studying mammalian perception, cognition and motor control.


Experimental Procedures
Sessions occurred during the day over the following =me frame: for the texture discrimina=on task three months throughout May, June and July 2017; for the size discrimina=on task three months during November, December and January 2017-2018; and finally for the brightness discrimina=on task, sampling took place over two months in February and March 2019. No significant altera=ons in Lo's whisker length took place between tasks (compare whisker lengths in example footage in Fig. 1). Pilot studies of each of the full discrimina=on tasks took place over three days prior to data collec=on to make sure the sea lion was fully desensi=sed to the experimental procedure, the apparatus and to check the posi=oning of the camera for whisker detec=on.
During the task, the same trainers were present on each occasion. The sea lion was blindfolded for both the texture and size discrimina=on task, but not for the brightness discrimina=on task. The sea lion was trained using posi=ve reinforcement, so if she successfully completed a trial, she received a fish reward. During a session, the sea lion received approximately 20% of her daily food amount. This was freshly thawed cut Atlan=c Mackerel (Scomber scombrus), Atlan=c Herring (Clupea harengus), or whole Capelin (Mallotus villosus) and European Sprat (Spra_us spra_us). A total of 30 days of footage was collected for the texture and size tasks and 20 days of footage for the visual brightness discrimina=on task (brightness). This gave 7200 trials (2700 for texture, 2700 for size and 1800 brightness trials).

Video selec4on and analysis
The GoPro Studio 2.0 programme (h_ps://gopro-studio.en.sobonic.com/) was used to remove the fisheye effect from the footage prior to video analysis. All trials were then examined to see if the video met the inclusion criteria for tracking: (i) all whiskers on both sides were visible for the Top-down Camera and all whiskers on one side were visible for the Side-on Camera, from approach to contact with the s=muli; (ii) the sea lion did not pre-emp=vely choose the target before the rig was placed in the water, (iii) the sea lion gave the correct answer. Aber viewing all the video footage, this gave a total of 805 individual interac=ons with one of the s=muli; 372 for the texture discrimina=on task (203 on the topdown camera and 169 on the side-on camera), 336 for the size discrimina=on task (193 on the top-down camera and 143 on the side-on camera) and 142 for the brightness discrimina=on task (75 on the top-down camera and 67 on the side-on camera). The number of s=mulus interac=ons for the visual brightness task was lower due to the sea lion rarely exploring the distractor s=muli. Details of tracking and sta=s=cal analyses can be found in the main manuscript text. Experimental set-up in the side-on (a) and top-down (b) view. The head (red points) and whiskers (blue points) were tracked from the video footage in two views as the sea lion explored each s=mulus. S=muli varied between the texture, size and visual brightness discrimina=on tasks, the target s=mulus for each task is indicated by the red asterisk (*). Whisker angular posi=ons were extracted from the tracking by calcula=ng the angle (θ) that the whiskers made with the midline of the head in both the side-on (c) and top-down views (d). Examples indicated here are for the right hand ventral whisker angle in the side-on view (green in panel c); and in the top-down view, the rostral whisker angle (yellow in panel d) and caudal whisker angles (green in panel d). Tracked whiskers in the top-down view included two rostral and two caudal whiskers (blue lines) from each side. Head movements were calculated during the s=muli explora=on in the side-on (g) and top-down view (h). Nose distance from the fish center was also calculated in the top-down view (panel f). Whisker amplitudes were calculated as the difference between the maximum whisker angular posi=on (green line θMAX at t=0) and the minimum whisker angular posi=on (green line θMIN at t=1) i.e. the difference between the most backward and most forward angular posi=on of that par=cular whisker within that individual s=mulus interac=on.

Fig. S3.
Supplementary results for mean angular posi0on from the three discrimina0on tasks. All graphs show median values with interquar=le ranges, and the asterisks (*) indicate significant differences (p<0.05) of tasks (red asterisks, next to the task headings) or s=muli, compared to other s=muli within the same task (black asterisk, above the error bars). There were significant differences (p<0.05) between all the tasks for mean angular posi=on in the side-on view, but not the top-down view.

Movie 1. Lo the California sea lion completing each of the three discrimination tasks.
Texture Discrimination Task: During the texture task, Lo made lateral, sweeping movements with her head and whiskers; Size Discrimination Task: During the size discrimination task Lo moved her nose and whiskers to the edges of a shape to judge its width; Brightness Discrimination Task: During the visual brightness task, head and whisker movements were greatly reduced and Lo usually went straight to the target stimulus using visual guidance.