Dissociated development of speech and limb sensorimotor learning in stuttering: speech auditory-motor learning is impaired in both children and adults who stutter

Stuttering is a neurodevelopmental disorder of speech fluency. Various experimental paradigms have demonstrated that affected individuals show limitations in sensorimotor control and learning. However, controversy exists regarding two core aspects of this perspective. First, it has been claimed that sensorimotor learning limitations are detectable only in adults who stutter (after years of coping with the disorder) but not during childhood close to the onset of stuttering. Second, it remains unclear whether stuttering individuals' sensorimotor learning limitations affect only speech movements or also unrelated effector systems involved in nonspeech movements. We report data from separate experiments investigating speech auditory-motor learning (N = 60) and limb visuomotor learning (N = 84) in both children and adults who stutter versus matched nonstuttering individuals. Both children and adults who stutter showed statistically significant limitations in speech auditory-motor adaptation with formant-shifted feedback. This limitation was more profound in children than in adults and in younger children versus older children. Between-group differences in the adaptation of reach movements performed with rotated visual feedback were subtle but statistically significant for adults. In children, even the nonstuttering groups showed limited visuomotor adaptation just like their stuttering peers. We conclude that sensorimotor learning is impaired in individuals who stutter, and that the ability for speech auditory-motor learning -- which was already adult-like in 3-6 year-old typically developing children -- is severely compromised in young children near the onset of stuttering. Thus, motor learning limitations may play an important role in the fundamental mechanisms contributing to the onset of this speech disorder.

Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex

System neuroscience of motor cognition regarding the space beyond immediate reach mandates free, yet experimentally controlled movements. We present an experimental environment (Reach Cage) and a versatile visuo-haptic interaction system (MaCaQuE) for investigating goal-directed whole-body movements of unrestrained monkeys. Two rhesus monkeys conducted instructed walk-and-reach movements towards targets flexibly positioned in the cage. We tracked 3D multi-joint arm and head movements using markerless motion capture. Movements show small trial-to-trial variability despite being unrestrained. We wirelessly recorded 192 broad-band neural signals from three cortical sensorimotor areas simultaneously. Single unit activity is selective for different reach and walk-and-reach movements. Walk-and-reach targets could be decoded from premotor and parietal but not motor cortical activity during movement planning. The Reach Cage allows systems-level sensorimotor neuroscience studies with full-body movements in a configurable 3D spatial setting with unrestrained monkeys. We conclude that the primate frontoparietal network encodes reach goals beyond immediate reach during movement planning.

Reaching around obstacles accounts for uncertainty in coordinate transformations

We show that changing body geometry such as head roll results in compensatory reaching behaviors around obstacles. Specifically, we observed head roll causes changed preferred movement direction and increased trajectory curvature. As has been shown before, head roll increases movement variability due to stochastic coordinate transformations. Thus these results provide evidence that the brain must consider the added movement variability caused by coordinate transformations for accurate reach movements.

Behavioral and Neural Variability of Naturalistic Arm Movements

Motor behaviors are central to many functions and dysfunctions of the brain, and understanding their neural basis has consequently been a major focus in neuroscience. However, most studies of motor behaviors have been restricted to artificial, repetitive paradigms, far removed from natural movements performed “in the wild.” Here, we leveraged recent advances in machine learning and computer vision to analyze intracranial recordings from 12 human subjects during thousands of spontaneous, unstructured arm reach movements, observed over several days for each subject. These naturalistic movements elicited cortical spectral power patterns consistent with findings from controlled paradigms, but with considerable neural variability across subjects and events. We modeled inter-event variability using ten behavioral and environmental features; the most important features explaining this variability were reach angle and day of recording. Our work is among the first studies connecting behavioral and neural variability across cortex in humans during unstructured movements and contributes to our understanding of long-term naturalistic behavior.

From competing motor plans to a single action within a single trial on the human motor periphery

ABSTRACTContemporary theories of motor control have suggested that multiple motor commands compete for action selection. While most of these competitions are completed prior to movement onset, averaged saccadic eye movements that land at an intermediate location between two visual targets are thought to arise when a movement is initiated prior to the resolution of the competition. In contrast, while averaged reach movements have been reported, there is still debate on whether averaged reach movements are the result of a resolved competition between two potential actions or a strategic behavior that optimally incorporates the current task demands. Here, we use a reach version of the paradigm that has previously shown to elicit saccadic averaging to examine whether similar averaging occurs based on neuromuscular activity of an upper limb muscle. On a single trial basis, we observed a temporal evolution of the two competing motor commands during a free-choice reach task to one of two visual targets. The initial wave of directionally-tuned muscle activity (∼100 ms after target onset) was an averaged of the two motor commands which then transformed into a single goal-directed motor command at the onset of the voluntary reach (∼200-300 ms after target onset). The transition from an early motor command to a single goal-direct command resembled the fact that saccadic averaging was most prominent for short-latency saccades. Further, the idiosyncratic choice made on a given trial was correlated with the biases in the averaged motor command.

Neck muscle spindle noise biases reaches in a multisensory integration task

Reference frame transformations (RFTs) are crucial components of sensorimotor transformations in the brain. Stochasticity in RFTs has been suggested to add noise to the transformed signal due to variability in transformation parameter estimates (e.g., angle) as well as the stochastic nature of computations in spiking networks of neurons. Here, we varied the RFT angle together with the associated variability and evaluated the behavioral impact in a reaching task that required variability-dependent visual-proprioceptive multisensory integration. Crucially, reaches were performed with the head either straight or rolled 30° to either shoulder, and we also applied neck loads of 0 or 1.8 kg (left or right) in a 3 × 3 design, resulting in different combinations of estimated head roll angle magnitude and variance required in RFTs. A novel three-dimensional stochastic model of multisensory integration across reference frames was fitted to the data and captured our main behavioral findings: 1) neck load biased head angle estimation across all head roll orientations, resulting in systematic shifts in reach errors; 2) increased neck muscle tone led to increased reach variability due to signal-dependent noise; and 3) both head roll and neck load created larger angular errors in reaches to visual targets away from the body compared with reaches toward the body. These results show that noise in muscle spindles and stochasticity in general have a tangible effect on RFTs underlying reach planning. Since RFTs are omnipresent in the brain, our results could have implications for processes as diverse as motor control, decision making, posture/balance control, and perception. NEW & NOTEWORTHY We show that increasing neck muscle tone systematically biases reach movements. A novel three-dimensional multisensory integration across reference frames model captures the data well and provides evidence that the brain must have online knowledge of full-body geometry together with the associated variability to plan reach movements accurately.

Modeling Hand Trajectories during Sequential Reach Movements in a Pulley Threading Task

Modeling of human motion is common in ergonomic analysis of industrial tasks and can help improve workplace design. We propose a method for modeling the trajectories of hand movements in the frontal plane during a sequential reach task that involves threading string through a system of pulleys. We model the motions as a combination of two consecutive phases, one where the hand is reaching between pulleys and another when the hand is engaged in threading a target pulley. Hand trajectories were modeled separately for each phase by fitting basis-splines to the observed data. Predicted trajectories were computed using task parameters as the input and compared to observed trajectories from the 12 participants who completed the study.

Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex

System neuroscience of motor cognition regarding the space beyond immediate reach mandates free, yet experimentally controlled movements. We present an experimental environment (Reach Cage) and a versatile visuo-haptic interaction system (MaCaQuE) for investigating goal-directed whole-body movements of unrestrained monkeys. Two rhesus monkeys conducted instructed walk-and-reach movements towards targets flexibly positioned in the cage. We tracked 3D multi-joint arm and head movements using markerless motion capture. Movements show small trial-to-trial variability despite being unrestrained. We wirelessly recorded 192 broad-band neural signals from three cortical sensorimotor areas simultaneously. Single unit activity is selective for different reach and walk-and-reach movements. Walk-and-reach targets could be decoded from premotor and parietal but not motor cortical activity during movement planning. The Reach Cage allows systems-level sensorimotor neuroscience studies with full-body movements in a configurable 3D spatial setting with unrestrained monkeys. We conclude that the primate frontoparietal network encodes reach goals beyond immediate reach during movement planning.