How a mouse licks a spout: Cortex-dependent corrections as the tongue reaches for, and misses, targets

Bollu, Tejapratap; B, Ito; Sc, Whitehead; Kardon, Brian; Redd, James; Mh, Liu; Goldberg, Jesse H.

doi:10.1101/655852

Cited by 9 publications

(8 citation statements)

References 34 publications

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“…Optogenetic inhibition of ALM impaired both the length of each lick and the ability to direct licks away from the midline. These results partly support recent work showing that inhibition of ALM impairs aspects of tongue kinematics in a cued-licking task 34 . Electrophysiological recordings in ALM revealed strong encoding of θ but surprisingly not L or L' (which can indirectly produce L ).…”

Section: Discussionsupporting

confidence: 90%

A functional cortical network for sensorimotor sequence generation

Chen

Delgado

et al. 2019

Preprint

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The brain generates complex sequences of movements that can be flexibly reconfigured in real-time based on sensory feedback, but how this occurs is not fully understood. We developed a novel 'sequence licking' task in which mice directed their tongue to a target that moved through a series of locations. Mice could rapidly reconfigure the sequence online based on tactile feedback. Closed-loop optogenetics and electrophysiology revealed that tongue/jaw regions of somatosensory (S1TJ) and motor (M1TJ) cortex encoded and controlled tongue kinematics at the level of individual licks. Tongue premotor (anterolateral motor, ALM) cortex encoded intended tongue angle in a smooth manner that spanned individual licks and even whole sequences, and progress toward the reward that marked successful sequence execution. ALM activity regulated sequence initiation, but multiple cortical areas collectively controlled termination of licking. Our results define a functional cortical network for hierarchical control of sensory-and reward-guided orofacial sequence generation.

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Section: Discussionsupporting

confidence: 90%

A functional cortical network for sensorimotor sequence generation

Chen

Delgado

et al. 2019

Preprint

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“…Manual dexterity of mice during food-handling interaction between the hands and orofacial apparatus. A future challenge is to understand how rapid, fine-scale movements of the tongue [31], teeth/jaws, lips, and other buccal musculature are orchestrated with those of the hands, and particularly the thumbs.…”

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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“…We demonstrated that CS and ALM had greater increases in calcium activity associated with body grooming than with face grooming (Fig.1, Fig.3), and our optogenetic stimulation paradigms often produced behaviors that resembled body grooming (turning inward towards the body and performing tongue movements), as opposed to face grooming (raising paws to face). This selectivity of CS for body grooming may reflect the known role of ALM in anticipatory and ingestive licking behavior in trained tasks that require consumption of liquid (Bollu et al, 2019;Li et al, 2015). Here, in an untrained context, we observed grooming and grooming-like behaviors that also involved licking.…”

Section: Specialization Of Alm-cs Circuit For Grooming May Partially mentioning

confidence: 53%

“…Prior work has demonstrated that anterior M2/anterior lateral motor area (ALM), one of the major cortical inputs to CS (Corbit et al, 2019), is associated both with appropriate sequencing of movements during trained tasks and with generating licking movements (Bollu et al, 2019;Li et al, 2015;Rothwell et al, 2015). ALM may therefore be uniquely suited for guiding selection of spontaneously generated behaviors such as body grooming.…”

Section: Alm Shows Increased Activity Specifically At Grooming Onsetmentioning

confidence: 99%

Dissociable roles of central striatum and anterior lateral motor area in initiating and sustaining naturalistic behavior

Corbit

Piantadosi

Wood

et al. 2020

Preprint

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Although much is known about how corticostriatal circuits mediate behavioral selection, most previous work has been conducted in highly trained animals engaged in instrumental tasks. Understanding how corticostriatal circuits mediate behavioral selection and initiation in a naturalistic setting is critical to understanding how the brain chooses and executes behavior in unconstrained situations. Central striatum (CS), an understudied region that lies in the middle of the motor-limbic topography, is well-poised to play an important role in these processes since its main cortical inputs (Corbit et al., 2019) have been implicated in behavioral flexibility (lateral orbitofrontal cortex (Kim and Ragozzino, 2005)) and response preparation (anterior lateral motor area, ALM) (Li et al., 2015), However, although CS activity has been associated with conditioned grooming behavior in transgenic mice (Burguiere et al., 2013), the role of CS and its cortical inputs in the selection of spontaneous behaviors has not been explored. We therefore studied the role of CS corticostriatal circuits in behavioral selection in an open field context. Surprisingly, using fiber photometry in this unconstrained environment, we found that population calcium activity in CS was specifically increased at onset of grooming, and not at onset of other spontaneous behaviors such as rearing or locomotion. Supporting a potential selective role for CS in the initiation of grooming, bilateral optogenetic stimulation of CS evoked immediate onset grooming-related movements. However, these movements resembled subcomponents of grooming behavior and not full-fledged grooming bouts, suggesting that additional input(s) are required to appropriately sequence and sustain this complex motor behavior once initiated. Consistent with this idea, optogenetic stimulation of CS inputs from ALM generated sustained grooming responses that evolved on a time-course paralleling CS activation monitored using single-cell calcium imaging. Furthermore, fiber photometry in ALM demonstrated a gradual ramp in calcium activity that peaked at time of grooming termination, supporting a potential role for ALM in encoding length of this spontaneous sequenced behavior.Finally, dual color dual region fiber photometry indicated that CS activation precedes ALM during naturalistic grooming sequences. Taken together, these data support a novel model in which CS activity is sufficient to initiate grooming behavior, but ALM activity is necessary to sustain and encode the length of grooming bouts. Thus, the use of an unconstrained behavioral paradigm has allowed us to uncover surprising roles for CS and ALM in the initiation and maintenance of spontaneous sequenced behaviors.

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How a mouse licks a spout: Cortex-dependent corrections as the tongue reaches for, and misses, targets

Cited by 9 publications

References 34 publications

A functional cortical network for sensorimotor sequence generation

A functional cortical network for sensorimotor sequence generation

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

Dissociable roles of central striatum and anterior lateral motor area in initiating and sustaining naturalistic behavior

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