Children with neurodevelopmental disorders, such as developmental coordination disorder (DCD), exhibit gross to fine sensorimotor impairments, reduced physical activity and interactions with the environment and people. This disorder co-exists with cognitive deficits, executive dysfunctions and learning impairments. Previously, we demonstrated in rats that limited amounts and atypical patterns of movements and somatosensory feedback during early movement restriction manifested in adulthood as degraded postural and locomotor abilities, and musculoskeletal histopathology, including muscle atrophy, hyperexcitability within sensorimotor circuitry and maladaptive cortical plasticity, leading to functional disorganization of the primary somatosensory and motor cortices in the absence of cortical histopathology. In this study, we asked how this developmental sensorimotor restriction (SMR) started to impact the integration of multisensory information and the emergence of sensorimotor reflexes in rats. We also questioned the enduring impact of SMR on motor activities, pain and memory. SMR led to deficits in the emergence of swimming and sensorimotor reflexes, the development of pain and altered locomotor patterns and posture with toe-walking, adult motor performance and night spontaneous activity. In addition, SMR induced exploratory hyperactivity, short-term impairments in object-recognition tasks and long-term deficits in object-location tasks. SMR rats displayed minor alterations in histological features of the hippocampus, entorhinal, perirhinal and postrhinal cortices yet no obvious changes in the prefrontal cortex. Taken all together, these results show similarities with the symptoms observed in children with DCD, although further exploration seems required to postulate whether developmental SMR corresponds to a rat model of DCD.

The dorsal striatum (dS) has been implicated in storing and retrieving procedural memories and controlling movement kinematics (e.g., speed). Since procedural memories are expressed through movements, the exact nature of the dS function has proven difficult to delineate. Here we challenged rats in complementary tasks designed to alleviate this performance confound. Surprisingly, dS lesions spared task-specific procedural memories but altered the kinematics of their expression in motor routines. Further behavioral analyses combined with simulations in the optimal control framework indicated that these alterations reflected an increased sensitivity to effort with preserved reward-seeking and ability to modulate movement speed. By setting the sensitivity to effort, the dS contributes to the optimization of the energy invested into voluntary movements. Such an elementary function of the dS might explain its implication in both procedural decisions and the control of movement speed.

The dorsal striatum (dS) has been implicated in storing procedural memories and controlling movement kinematics. Since procedural memories are expressed through movements, the exact nature of the dS function has proven difficult to delineate. Here, we challenged rats in complementary locomotion-based tasks designed to alleviate this confound. Surprisingly, dS lesions did not impair the rats' ability to remember the procedure for the successful completion of motor routines. However, the speed and initiation of the reward-oriented phase of the routines were irreversibly altered by the dS lesion. Further behavioral analyses, combined with modeling in the optimal control framework, indicated that these kinematic alterations were well explained by an increased sensitivity to effort. Our work provides evidence supporting a primary role of the dS in modulating the kinematics of reward-oriented actions, a function that may be related to the optimization of the energetic costs of moving.

How animals adapt their behavior according to regular time intervals between events is not well understood, especially when intervals last several seconds. One possibility is that animals use disembodied internal neuronal representations of time to decide when to initiate a given action at the end of an interval. However, animals rarely remain immobile during time intervals but tend to perform stereotyped behaviors, raising the possibility that motor routines improve timing accuracy. To test this possibility, we used a task in which rats, freely moving on a motorized treadmill, could obtain a reward if they approached it after a fixed interval. Most animals took advantage of the treadmill length and its moving direction to develop, by trial-and-error, the same motor routine whose execution resulted in the precise timing of their reward approaches. Noticeably, when proficient animals did not follow this routine, their temporal accuracy decreased. Then, naïve animals were trained in modified versions of the task designed to prevent the development of this routine. Compared to rats trained in the first protocol, these animals didn’t reach a comparable level of timing accuracy. Altogether, our results indicate that timing accuracy in rats is improved when the environment affords cues that animals can incorporate into motor routines.

How animals adapt their movements to take advantage of behaviorally-relevant time intervals is not well understood, especially in the supra-second timescale. It has been proposed that motor timing depends on the emergence of self-sustained dynamics across ensembles of neurons. Alternatively, evidence from operant conditioning suggests that animals can develop motor routines to adapt their behavior to fixed temporal constraints. But it is unclear whether animals can accurately time their behavior without the help of motor routines. To address this issue, we used a task in which rats, freely moving on a motorized treadmill, could obtain a reward if they approached it after a fixed interval. Most animals took advantage of the treadmill length and its moving direction to develop, by trial-and-error, a unique motor routine whose execution resulted in the precise timing of their reward approaches. Noticeably, when proficient animals occasionally failed to follow this routine, the timing of their reward approaches was systematically poor. In a second step, we trained naive animals in modified versions of the task specifically designed to prevent the development of this motor strategy. Compared to rats trained in the first protocol, these animals never reached a comparable level of timing accuracy. We conclude that motor timing critically depends on the ability of animals to develop motor routines adapted to the structure of their environment. Our work also suggests that self-sustained neuronal activity alone may not be sufficient to support motor timing, at least in the supra-second timescale.