Distinct dynamics of neuronal activity during concurrent motor planning and execution

The smooth conduct of movements requires simultaneous motor planning and execution according to internal goals. So far it remains unknown how such movement plans are modified without interfering with ongoing movements. Previous studies have isolated planning and execution-related neuronal activity by separating behavioral planning and movement periods in time by sensory cues. Here, we separate continuous self-paced motor planning from motor execution statistically, by experimentally minimizing the repetitiveness of the movements. This approach shows that, in the rat sensorimotor cortex, neuronal motor planning processes evolve with slower dynamics than movement-related responses. Fast-evolving neuronal activity precees skilled forelimb movements and is nested within slower dynamics. We capture this effect via high-pass filtering and confirm the results with optogenetic stimulations. The various dynamics combined with adaptation-based high-pass filtering provide a simple principle for separating concurrent motor planning and execution.

Cortical activity at different time scales: high‐pass filtering separates motor planning and execution

The smooth conduction of movements requires simultaneous motor planning and execution according to internal goals. So far it is not known how such movement plans can be modified without being distorted by ongoing movements. Previous studies have isolated planning and execution related neuronal activity by separating behavioral planning and movement periods in time by sensory cues1–7. Here, we introduced two novel tasks in which motor planning developed intrinsically. We separated this continuous self-paced motor planning statistically from motor execution by experimentally minimizing the repetitiveness of the movements. Thereby, we found that in the rat sensorimotor cortex, neuronal motor planning processes evolved with slower dynamics than movement related responses both on a sorted unit and population level. The fast evolving neuronal activity preceded skilled forelimb movements while it coincided with movements in a locomotor task. We captured this fast evolving movement related activity via a high-pass filter approach and confirmed the results with optogenetic stimulations. As biological mechanism underlying such a high pass filtering we suggest neuronal adaption. The differences in dynamics combined with a high pass filtering mechanism represents a simple principle for concurrent motor planning and execution in which planning will result in relatively slow dynamics that will not produce movements.

RATS: A Robotic Arm Training System Designed for Rats

This paper presents a novel robotic system to characterize and retrain reaching in rats. This robot is intended to be a research platform for rehabilitation of forelimb movements in rats. In this paper, we focus on the design of this robotic system. We present the design requirements, mathematical models, and details of the physical device. A parallel mechanism with a special alignment of the component chains is used to accommodate observed reaching motions of a rat's forelimb. Additionally, we demonstrate the use of this robot to record forelimb trajectories. Three healthy rats were used to record repeated reaching motions while the robot applied nearly zero force. We believe that this robotic system can be used in future training studies with rats who have impaired arm motions due to a neurological insult.

Descending neocortical output critical for skilled forelimb movements is distributed across projection cell classes

Motor cortex is a key node in the forebrain circuits that enable flexible control of limb movements. The influence of motor cortex on movement execution is primarily carried by either pyramidal tract neurons (PT), which project directly to the brainstem and spinal cord, or intratelencephalic neurons (IT), which project within the forebrain. The logic of the interplay between these cell types and their relative contribution to the coordination and scaling of forelimb movements remains unclear. Here we combine large-scale neural recordings across all layers of motor cortex with cell-type specific perturbations in a cortex-dependent mouse behavior: kinematically-variable manipulation of a joystick. Our data demonstrate that descending neocortical motor commands are distributed across projection cell classes. IT neuron activity, in comparison to PT neurons, carries a larger fraction of information about gross movement kinematics. We find that forelimb movements are robust to optogenetic silencing of PT output, but substantially impaired by silencing Layer 5a IT projection neurons. Dorsal striatum is the unique extracortical integration point for IT and PT output pathways and its activity was more dependent upon IT input than PT input during movement execution. These data indicate that forebrain extrapyramidal pathways can be critical for regulating kinematics of motor skills.

Sensory coding of limb kinematics in developing primary motor cortex

Primary motor cortex (M1) undergoes protracted development in rodents, functioning initially as a sensory structure. As we reported previously in neonatal rats (Dooley and Blumberg, 2018), self-generated forelimb movements—especially the twitch movements that occur during active sleep—trigger sensory feedback (reafference) that strongly activates M1. Here, we expand our investigation by using a video-based approach to quantify the kinematic features of forelimb movements with sufficient precision to reveal receptive-field properties of individual M1 units. At postnatal day (P) 8, nearly all M1 units were strongly modulated by movement amplitude, but only during active sleep. By P12, the majority of M1 units no longer exhibited amplitude-dependence, regardless of sleepwake state. At both ages, movement direction produced changes in M1 activity, but to a much lesser extent than did movement amplitude. Finally, we observed that population spiking activity in M1 becomes more continuous and decorrelated between P8 and P12. Altogether, these findings reveal that M1 undergoes a sudden transition in its receptive field properties and population-level activity during the second postnatal week. This transition marks the onset of the next stage in M1 development before the emergence of its later-emerging capacity to influence motor outflow.

RATS: A Robotic Arm Training System Designed for Rats

This paper presents a novel robotic system to characterize and retrain reaching in rats. This robot is intended to be a research platform for rehabilitation of forelimb movements in rats. In this paper, we focus on the design of this robotic system. We present the design requirements, mathematical models, and details of the physical device. A parallel mechanism with a special alignment of the component chains is used to accommodate observed reaching motions of a rat’s forelimb. Additionally, we demonstrate the use of this robot to record forelimb trajectories. Three healthy rats were used to record repeated reaching motions while the robot applied nearly zero force. We believe that this robotic system can be used in future training studies with rats who have impaired arm motions due to a neurological insult.

Prey speed influences the speed and structure of the raptorial strike of a ‘sit-and-wait’ predator

Predators must often employ flexible strategies to capture prey. Particular attention has been given to the strategies of visual predators that actively pursue their prey, but sit-and-wait predators have been largely overlooked, their strategies often characterized as stereotyped. Praying mantids are primarily sit-and-wait predators that often employ crypsis to catch their prey using a raptorial strike produced by their highly modified forelimbs. Here, we show that the raptorial strike of the Madagascan marbled mantis ( Polyspilota aeruginosa ) varies in duration from 60 to 290 ms due to the tibial extension alone; slower strikes involve slower tibial extensions that may also be interrupted by a pause. The success of a strike is independent of its duration or the presence of these pauses. However, prey speed affects the duration of tibial extension and the probability of a pause occurring, both increasing at slower prey speeds. Adjusting the duration of the tibial extension according to prey speed allows mantids to time the final downward sweep of the tibia to their prey's approach. The use of visual inputs to adjust the motor pattern controlling forelimb movements shows that not all aspects of the strike are stereotyped and that sit-and-wait predators can produce behavioural flexibility.

Interhemispheric modulations of motor outputs by the rostral and caudal forelimb areas in rats

In rats, forelimb movements are evoked from two cortical regions, the caudal and rostral forelimb areas (CFA and RFA, respectively). These areas are densely interconnected and RFA induces complex and powerful modulations of CFA outputs. CFA and RFA also have interhemispheric connections, and these areas from both hemispheres send projections to common targets along the motor axis, providing multiple potential sites of interactions for movement production. Our objective was to characterize how CFA and RFA in one hemisphere can modulate motor outputs of the opposite hemisphere. To do so, we used paired-pulse protocols with intracortical microstimulation techniques (ICMS), while recording electromyographic (EMG) activity of forelimb muscles in sedated rats. A subthreshold conditioning stimulation was applied in either CFA or RFA in one hemisphere simultaneously or before a suprathreshold test stimulation in either CFA or RFA in the opposite hemisphere. Both CFA and RFA tended to facilitate motor outputs with short (0–2.5 ms) or long (20–35 ms) delays between the conditioning and test stimuli. In contrast, they tended to inhibit motor outputs with intermediate delays, in particular 10 ms. When comparing the two areas, we found that facilitatory effects from RFA were more frequent and powerful than the ones from CFA. In contrast, inhibitory effects from CFA on its homolog were more frequent and powerful than the ones from RFA. Our results demonstrate that interhemispheric modulations from CFA and RFA share some similarities but also have clear differences that could sustain specific functions these cortical areas carry for the generation of forelimb movements. NEW & NOTEWORTHY We show that caudal and rostral forelimb areas (CFA and RFA) have distinct effects on motor outputs from the opposite hemisphere, supporting that they are distinct nodes in the motor network of rats. However, the pattern of interhemispheric modulations from RFA has no clear equivalent among premotor areas in nonhuman primates, suggesting they contribute differently to the generation of ipsilateral hand movements. Understanding these interspecies differences is important given the common use of rodent models in motor control and recovery studies.

Forelimb movements evoked by optogenetic stimulation of the macaque motor cortex

Optogenetics has become an indispensable tool for investigating brain functions. Although non-human primates are particularly useful models for understanding the functions and dysfunctions of the human brain, application of optogenetics to non-human primates is still limited. In the present study, we generated an effective adeno-associated viral vector serotype DJ to express channelrhodopsin-2 (ChR2) under the control of a strong ubiquitous CAG promoter and injected into the somatotopically identified forelimb region of the primary motor cortex in macaque monkeys. ChR2 was strongly expressed around the injection sites, and optogenetic intracortical microstimulation (oICMS) through a homemade optrode induced prominent cortical activity: Even single-pulse, short duration oICMS evoked long-lasting repetitive firings of cortical neurons. In addition, oICMS elicited distinct forelimb movements and muscle activity, which were comparable to those elicited by conventional electrical ICMS. The present study removed obstacles to optogenetic manipulation of neuronal activity and behaviors in non-human primates.