The syntactic organization of pasta-eating and the structure of reach movements in the head-fixed mouse

Whishaw, Ian Q.; Faraji, Jamshid; Kuntz, Jessica R.; Agha, Behroo Mirza; Metz, Gerlinde A. S.; Mohajerani, Majid H.

doi:10.1038/s41598-017-10796-y

Cited by 27 publications

(16 citation statements)

References 45 publications

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“…Results from several studies of rats suggest that the symmetry/asymmetry of forelimb movements during food-handling reflects the particular geometry of the food (e.g. pasta) [10,[28][29][30].…”

Section: Discussionmentioning

confidence: 99%

Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements

2020

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The small first digit (D1) of the mouse's hand resembles a volar pad, but its thumb-like anatomy suggests ethological importance for manipulating small objects. To explore this possibility, we recorded high-speed close-up video of mice eating seeds and other food items. Analyses of ethograms and automated tracking with DeepLabCut revealed multiple distinct microstructural features of food-handling. First, we found that mice indeed made extensive use of D1 for dexterous manipulations. In particular, mice used D1 to hold food with either of two grip types: a pincer-type grasp, or a "thumb-hold" grip, pressing with D1 from the side. Thumb-holding was preferentially used for handling smaller items, with the smallest items held between the two D1s alone. Second, we observed that mice cycled rapidly between two postural modes while feeding, with the hands positioned either at the mouth (oromanual phase) or resting below (holding phase). Third, we identified two highly stereotyped D1related movements during feeding, including an extraordinarily fast (~20 ms) "regrip" maneuver, and a fast (~100 ms) "sniff" maneuver. Lastly, in addition to these characteristic simpler movements and postures, we also observed highly complex movements, including rapid D1-assisted rotations of food items and dexterous simultaneous double-gripping of two food fragments. Manipulation behaviors were generally conserved for different food types, and for head-fixed mice. Wild squirrels displayed a similar repertoire of D1-related movements. Our results define, for the mouse, a set of kinematic building-blocks of manual dexterity, and reveal an outsized role for D1 in these actions. OPEN ACCESSCitation: Barrett JM, Raineri Tapies MG, Shepherd GMG (2020) Manual dexterity of mice during foodhandling involves the thumb and a set of fast basic movements. PLoS ONE 15(1): e0226774. https://

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Section: Discussionmentioning

confidence: 99%

Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements

2020

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“…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.…”

Section: Introductionmentioning

confidence: 99%

A kinematic study of skilled reaching movement in rat

Parmiani

Lucchetti

Bonifazzi

et al. 2019

Journal of Neuroscience Methods

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Background: In the rat, the single-pellet reaching task includes orienting, reaching, grasping and retracting movements. It has previously been described by notation techniques, high-speed video and cineradiographic recordings. Recently, high-definition cameras have been used to track paw and digit movements with DeepLabCut, a machine-learning algorithm for markerless estimation of paw position. New method: Our new approach consists of positioning three high-speed infrared digital cameras to track the full motion of markers on the rat's body. This provided a previously unavailable 3D recording of skilled reaching kinematics in the rat moving freely in the reaching box, which were analysed by Qualisys Track Manager software and MATLAB. Results: This method enabled description of kinematic parameters unobtainable without motion tracking and provided insight into the spatiotemporal metrics of movements used to perform skilled reaching. It revealed that orientation features three steps and reaching has two bimodal start-point distributions, one along the horizontal axis and one along the vertical axis. At the end of reaching, the wrist/paw occupies the same position as the nose at the end of orienting. In grasping, averaging trajectories confirmed the marker lowering and target approaching. Comparison with existing methods: Our method required significantly reduced time to label data and obviates the need for off-line manual marking of videos. It provides an efficient means of capturing volumes containing the entire range of marker movements. Conclusions: This study validated a new and efficient approach for quantifying rat movement kinematics, useful for comparing preclinical and clinical conditions.

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“…This increases the labor and time needed to perform experiments, and so systematically testing of stimulation paradigms has been largely relegated to simpler metrics (Porter et al, 2012; Hays et al, 2014; Hulsey et al, 2019). These more complex behaviors also usually come at the cost of gathering detailed quantitative metrics, limiting their analysis of behavioral outcomes to qualitative metrics (Whishaw et al, 2008, 2017). Other systems have succeeded in automation but lack closed-loop stimulation (Williamson et al, 2018; Fenrich et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Closed-loop automated reaching apparatus (CLARA) for interrogating motor systems

Bowles

Williamson

Nettles

et al. 2021

Preprint

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Objective: Personalized neurostimulation is a rapidly expanding category of therapeutics for a broad range of indications. Development of these innovative neurological devices requires high-throughput systems for closed-loop stimulation of model organisms, while monitoring physiological signals and complex, naturalistic behaviors. To address this need, we developed CLARA, a closed-loop automated reaching apparatus. Approach: Using breakthroughs in computer vision, CLARA integrates fully-automated, markerless kinematic tracking of multiple features we use to classify animal behavior and precisely deliver neural stimulation based on behavioral outcomes. CLARA is compatible with advanced neurophysiological tools, enabling the testing of neurostimulation devices and identification of novel neurological biomarkers. Results: The CLARA system tracks unconstrained skilled reach behavior in 3D at 150hz without physical markers. The system fully automates trial initiation and pellet delivery and is capable of accurately delivering stimulation in response to trial outcome with sub-quarter second latency. Mice perform the skilled reach task in the CLARA system at a proficiency similar to manually trained animals. Kinematic data from the CLARA system provided novel insights into the dynamics of reach consistency over the course of learning, suggesting that changes are driven entirely by unsuccessful reach accuracy. Additionally, using the closed-loop capabilities of CLARA, we demonstrate that vagus nerve stimulation (VNS) delivered on reach success improves skilled reach performance and increases reach trajectory consistency in healthy animals. Significance: The CLARA system is the first mouse behavior apparatus that uses markerless pose tracking to provide real-time closed-loop stimulation in response to the outcome of an unconstrained motor task. Additionally, we demonstrate that the CLARA system was essential for our finding that VNS given after successful completion of a motor task improves performance in healthy animals. This approach has high translational relevance for developing neurostimulation technology based on complex human behavior.

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The syntactic organization of pasta-eating and the structure of reach movements in the head-fixed mouse

Cited by 27 publications

References 45 publications

Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements

Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements

A kinematic study of skilled reaching movement in rat

Closed-loop automated reaching apparatus (CLARA) for interrogating motor systems

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