A robust role for motor cortex

Abstract

The role of motor cortex in non-primate mammals remains unclear. More than a 10 century of stimulation, anatomical and electrophysiological studies has implicated neural activity in 11 this region with all kinds of movement. However, following the removal of motor cortex, rats retain 12 most of their adaptive behaviours, including previously learned skilled movements. Here we revisit 13 these two conflicting views of motor cortex and present a new behaviour assay, challenging 14 animals to respond to unexpected situations while navigating a dynamic obstacle course.15 Surprisingly, rats with motor cortical lesions show clear impairments facing an unexpected collapse 16 of the obstacles, while showing no impairment with repeated trials in many motor and cognitive 17 metrics of performance. We propose a new role for motor cortex: extending the robustness of 18 sub-cortical movement systems, specifically to unexpected situations demanding rapid motor 19 responses adapted to environmental context. The implications of this idea for current and future 20 research are discussed. 21 22 45 the other. He connected the orderly march of these spasms to the existence of localized lesions in 46 the post-mortem brain of his patients and hypothesized that the origin of these fits was uncontrolled 47 excitation caused by local changes in cortical grey matter (Jackson, 1870). In that same year, Fritsch 48 and Hitzig published their famous study demonstrating that it is possible to elicit movements by 49 direct stimulation of the cortex in dogs (Fritsch and Hitzig, 1870). Furthermore, stimulation of 50 different parts of the cortex produced movement in different parts of the body (Fritsch and Hitzig, 51 1870). It appeared that the causal mechanism for epileptic convulsions predicted by Hughlings 52 Jackson had been found, and with it a possible explanation for how the intact brain might control 53 movement. The cerebral cortex was already considered at the time to be the seat of reasoning 54 and sensation, so if activity over this so-called motor cortex was able to exert direct control over the 55 musculature of the body, then it might, in the normal brain, be the area that connects volition to 56 muscles (Fritsch and Hitzig, 1870). The Goltz-Ferrier debates 58 David Ferrier, a Scottish neurologist deeply impressed by the ideas of Hughlings Jackson and by the 59 positive results of Fritsch and Hitzig's experiments, proceeded to reproduce and expand on their 60 observations with comprehensive stimulation studies showing how activity in the motor cortex 61 was sufficient to produce a large variety of movements across a wide range of mammalian species 62 (Ferrier, 1873). Meanwhile, other researchers across Europe such as Goltz and Christiani were 63 facing a dilemma: in many of the so-called "lower mammals" massive lesions of the cerebral cortex 64 failed to demonstrate any visible long-term impairments in the motor behaviour of animals (James, 65 1885; Goltz, 1888). These two lines of inquiry first clashed at the seventh Inte...

Behaviorally Selective Engagement of Short-Latency Effector Pathways by Motor Cortex

“…This variation in motor cortical influence suggests that the specificity of behavioral deficits following lesions or pharmacological inactivation that eliminate motor cortical output does not merely reflect an inability of other motor areas to compensate during a subset of movements. Moreover, the agreement between the latencies of silencing effects during precision pull and of stimulation responses implies a direct influence of motor cortical output on muscle activity in rodents, contrary to recent claims (Lopes et al, 2016). …”

Mouse Motor Cortex Coordinates the Behavioral Response to Unpredicted Sensory Feedback

“…Cortical control of movement may therefore have co-evolved with an increasing reliance of species on cortical processing of sensory input providing the necessary information to guide movement with accuracy and precision, especially when the extraction of sensory information requires complex processing. In agreement with such a model, effects of motor cortex lesion in rodents are most pronounced when the task requires fine digit control ( Whishaw et al., 1998 ), when animals encounter novel sensory conditions and movement coordination requires rapid sensory feedback control ( Lopes et al., 2016 ), or when animals are still in the process of learning to control the movement ( Kawai et al., 2015 ). It is thus conceivable that motor cortex functions to structure and adjust movements based on incoming sensory information processed in cortex.…”

“…Mouse visual cortex, for example, is thought to not only process visual information, but also act as a detector of visual feedback that deviates from the visual feedback based on motor output ( Attinger et al., 2017 , Fiser et al., 2016 , Zmarz and Keller, 2016 ). Consistent with the hypothesis that motor cortex might be involved in the processing of deviations of expected from actual sensory input, selective responses triggered by unexpected feedback perturbations during locomotion are present in cat motor cortex ( Marple-Horvat et al., 1993 ), and in rodents it has been shown that motor cortex is necessary for the rapid initiation of a behavioral response to an unexpected feedback perturbation ( Lopes et al., 2016 ). Moreover, exposing animals to increased demands for movement accuracy results in increased activity in motor cortex, which could be the consequence of increased precision in sensory feedback guided control of movement ( Beloozerova et al., 2010 , Beloozerova and Sirota, 1993b , Farrell et al., 2015 ).…”

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

“…Our results suggest that the utility of this BG pathway can be extended to generate novel task-specific motor sequences -a process that may require a motor cortex-dependent reprogramming of subcortical motor circuits. This would allow cortex to off-load the 'task' of generating specialized and stereotyped learned behaviors to subcortical circuits, making them more automatized and less prone to cortical 'interference' 126 . Consistent with this idea are observations that task-related cortical activity decreases over the course of training and with increasing automaticity 27,[127][128][129][130][131][132][133] .…”