Organization of the reach and grasp in head-fixed vs freely-moving mice provides support for multiple motor channel theory of neocortical organization

Abstract

Multiple motor channel (MMC) theory of neocortical organization proposes that complex movements, such as reaching for a food item to eat, are produced by the coordinated action of separate neural channels. For example, the human reach-to-grasp act is mediated by two visuo-parieto-motor cortex channels, one for the reach and one for the grasp. The present analysis asked whether there is a similar organization of reach-and-grasp movements in the mouse. The reach-to-eat movements of the same mice were examined from high-shutter speed, frame-by-frame video analysis in three tasks in which the mice obtained equivalent success scores: when freely-moving reaching for food pellets, when head-fixed reaching for food pellets, and when head-fixed reaching for pieces of pasta. To reach, the mice used egocentric cues to vary upper arm movements in a task-appropriate manner to place an open hand on the food or to locate the food using a "touch-release-grasp" strategy. Although mice could not hand-shape offline when reaching, they could hand-shape using online touch-related cues from the mouth to manipulate the food at the mouth. That the reach can be performed offline in relation to egocentric cues whereas hand shaping for the grasp requires online cues supports the idea that for the mouse, as for primates, the reach and grasp are separate acts. The results are further discussed in relation to the use of the head-fixed behavioral procedure to identify the independent neural substrates of the reach and the grasp using mesoscale stimulation/imaging methods.

Quantification of Mouse Reach Kinematics as a Foundation for Mechanistic Interrogation of Motor Control

“…First, we found that reach endpoint appears to be actively regulated in trials in which animals make several attempts during a single reach. A previous study reported multiple-attempt reaches in head-fixed mice, describing a touchrelease-grab sequence in which the initial attempt involves "semi-flexed and semi-closed digits" (Whishaw et al, 2017). We extended this observation by analyzing endpoints on subsequent reach attempts, finding that the mean distance from the target decreased from first to second attempts with no significant difference in endpoint variability.…”

“…Thus, charting similarities and differences in basic kinematic measurements across behavioral contexts and across species can provide stepping stones for future experiments aimed at uncovering neural mechanisms into how the nervous system produces reach behavior. Although some prior studies quantified aspects of mouse reach kinematics, the majority focused mainly on success rates, qualitative descriptions and scoring systems, or categorical demarcation of the reach into phases, with few explicit connections drawn to the kinematic control principles discussed here (Esposito et al, 2014;Farr & Whishaw, 2002;Galiñanes et al, 2018b;Guo et al, 2015;Whishaw, 1996;Whishaw et al, 2017Whishaw et al, , 2018Whishaw & Pellis, 1990). This study establishes several basic quantitative frameworks for analyzing mouse reach kinematics, allowing numerical comparisons to be drawn across species and across tasks.…”

“…Motor behavior is strongly influenced by the context in which it is performed. Previous work identified qualitative differences in the behavioral patterns of reach-to-grasp movements in mice that were head-fixed, compared to freely-behaving animals, but whether these differences extend to the level of reach kinematics remains unclear (Whishaw et al, 2017). We therefore sought to test the degree to which the intrinsic kinematic relationships defined above are altered by the experimental constraint of head-fixation, a relatively common experimental method ( Figure 8A-C).…”

“…Compared to the freely-behaving condition, head-fixed reaches displayed an early upward velocity peak that dominated the speed profile, resulting in high asymmetry. If early peaks in upward velocity correspond to an initial 'aiming' phase separate from the 'transport' phase, it could represent an altered control strategy interacting with the constraints of head-fixation (Whishaw et al, 1992(Whishaw et al, , 2017. Ultimately, these similarities and differences in basic kinematic features represent compelling avenues for further exploration of species-and task-specific constraints on reach control.…”

Low acetylcholine during early sleep is important for motor memory consolidation

“…To assess the effect of physostigmine injections on the quality of reaches, the video recordings on day 9 , from the first 3 reaches, 12 components of movements were scored on a 0, 0.5, and 1 scale (good, impaired, and absent performance). A higher score thus indicates inferior performance (Whishaw IQ et al 2008;Whishaw IQ et al 2017). To compare scores of the two groups, we performed repeated measures ANOVA with Treatment (Saline or Physostigmine) and Sex as "between-subjects" factors and Movement Inayat_and_Qandeel et al 2019…”