Negative optokinetic afternystagmus in larval zebrafish demonstrates set-point adaptation

Motor learning is essential to maintain accurate behavioral responses. We used a larval zebrafish model to study ocular motor learning behaviors. During a sustained period of optokinetic stimulation in 5-day-old wild-type zebrafish larvae the slow-phase eye velocity decreased over time. Then interestingly, a long-lasting and robust negative optokinetic afternystagmus (OKAN) was evoked upon light extinction. The slow-phase velocity, the quick-phase frequency, and the decay time constant of the negative OKAN were dependent on the stimulus duration and the adaptation to the preceding optokinetic stimulation. Based on these results, we propose a sensory adaptation process during continued optokinetic stimulation, which, when the stimulus is removed, leads to a negative OKAN as the result of a changed retinal slip velocity set point, and thus, a sensorimotor memory. The pronounced negative OKAN in larval zebrafish not only provides a practical solution to the hitherto unsolved problems of observing negative OKAN, but also, and most importantly, can be readily applied as a powerful model for studying sensorimotor learning and memory in vertebrates.

Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation

Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW & NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces.

Sensorimotor Memory for Object Weight is Based on Previous Experience During Lifting, Not Holding

ABSTRACTTo allow skilled object manipulation, the brain must generate a motor command specifically tailored to the object properties. For instance, in object lifting, the forces applied by the fingertips must be scaled to the object’s weight. When lifting a series of objects, forces are usually scaled according to recent experience from previously lifted objects, an effect often referred to as sensorimotor memory. In this study, we investigated the specific time period during which stored information from previous object manipulation is used to mediate sensorimotor memory. More specifically, we examined whether sensorimotor memory was based on weight information obtained between object contact and lift completion (lifting phase) or during stable holding (holding phase). Participants lifted objects in virtual reality that could increase or decrease in weight after the object was lifted and held in the air. In this way, we could distinguish whether the force planning in the next lift was scaled depending on weight information gathered from either the dynamic lifting or static holding period. We found that force planning was based on the previous object weight experienced during the lifting, but not holding, phase. This suggest that the lifting phase, while merely lasting a few hundred milliseconds, is a key time period for building up internal object representations used for planning future hand-object interactions.HIGHLIGHTSWhen lifting objects, fingertip force scaling is based on the most recent liftWe investigated what time period is critical for acquiring sensorimotor memorySensorimotor memory is based on weight experienced during previous lift, not holdThe lifting phase is a key period for building up internal models of object lifting

Infants’ prospective control during object manipulation in an uncertain environment

This study investigates how infants use visual and sensorimotor information to prospectively control their actions. We gave 14-month-olds two objects of different weight and observed how high they were lifted, using a Qualisys Motion Capture System. In one condition, the two objects were visually distinct (different color condition) in another they were visually identical (same color condition). Lifting amplitudes of the first movement unit were analyzed in order to assess prospective control. Results demonstrate that infants lifted a light object higher than a heavy object, especially when vision could be used to assess weight (different color condition). When being confronted with two visually identical objects of different weight (same color condition), infants showed a different lifting pattern than what could be observed in the different color condition, expressed by a significant interaction effect between object weight and color condition on lifting amplitude. These results indicate that (a) visual information about object weight can be used to prospectively control lifting actions and that (b) infants are able to prospectively control their lifting actions even without visual information about object weight. We argue that infants, in the absence of reliable visual information about object weight, heighten their dependence on non-visual information (tactile, sensorimotor memory) in order to estimate weight and pre-adjust their lifting actions in a prospective manner.

Causal explanation of individual differences in human sensorimotor memory formation

Sensorimotor cortex mediates the formation of adaptation memory. Individuals differ in the rate at which they acquire, retain, and generalize adaptation. We present a mechanistic explanation of the neurochemical and computational causes of this variation in humans. Neuroimaging identified structural, functional and neurochemical covariates of a computational parameter that determines memory persistence. To establish causality, we increased sensorimotor cortex excitability during adaptation, using transcranial direct current stimulation. As predicted, this increased retention. Inter-individual variance in the stimulation-induced E:I increase predicted the computational change, which predicted the memory gain. These relations did not hold, and memory was unchanged, with stimulation applied before adaptation. This cognitive state dependent effect was modulated by the BDNF val66met genetic polymorphism. Memory was enhanced by stimulation in Val/Val carriers only, implicating a mechanistic role for activity-dependent BDNF secretion. Sensorimotor cortex E:I causally determines the time constant of memory persistence, explaining phenotypic variation in adaptation decay.

Representing multiple object weights: competing priors and sensorimotor memories

When lifting an object, individuals scale lifting forces based on long-term priors relating external object properties (such as material and size) to object weight. When experiencing objects that are poorly predicted by priors, people rapidly form and update sensorimotor memories that can be used to predict an object's atypical size-weight relation in support of predictively scaling lift forces. With extensive experience in lifting such objects, long-term priors, assessed with weight judgments, are gradually updated. The aim of the present study was to understand the formation and updating of these memory processes. Participants lifted, over multiple days, a set of black cubes with a normal size-weight mapping and green cubes with an inverse size-weight mapping. Sensorimotor memory was assessed with lifting forces, and priors associated with the black and green cubes were assessed with the size-weight illusion (SWI). Interference was observed in terms of adaptation of the SWI, indicating that priors were not independently adjusted. Half of the participants rapidly learned to scale lift forces appropriately, whereas reduced learning was observed in the others, suggesting that individual differences may be affecting sensorimotor memory abilities. A follow-up experiment showed that lifting forces are not accurately scaled to objects when concurrently performing a visuomotor association task, suggesting that sensorimotor memory formation involves cognitive resources to instantiate the mapping between object identity and weight, potentially explaining the results of experiment 1. These results provide novel insight into the formation and updating of sensorimotor memories and provide support for the independent adjustment of sensorimotor memory and priors.

Fast-adapting mechanoreceptors are important for force control in precision grip but not for sensorimotor memory

Sensory feedback from cutaneous mechanoreceptors in the fingertips is important in effective object manipulation, allowing appropriate scaling of grip and load forces during precision grip. However, the role of mechanoreceptor subtypes in these tasks remains incompletely understood. To address this issue, psychophysical tasks that may specifically assess function of type I fast-adapting (FAI) and slowly adapting (SAI) mechanoreceptors were used with object manipulation experiments to examine the regulation of grip force control in an experimental model of graded reduction in tactile sensitivity (healthy volunteers wearing 2 layers of latex gloves). With gloves, tactile sensitivity decreased significantly from 1.9 ± 0.4 to 12.3 ± 2.2 μm in the Bumps task assessing function of FAI afferents but not in a grating orientation task assessing SAI afferents (1.6 ± 0.1 to 1.8 ± 0.2 mm). Six axis force/torque sensors measured peak grip (PGF) and load (PLF) forces generated by the fingertips during a grip-lift task. With gloves there was a significant increase of PGF (14 ± 6%), PLF (17 ± 5%), and grip and load force rates (26 ± 8%, 20 ± 8%). A variable-weight series task was used to examine sensorimotor memory. There was a 20% increase in PGF when the lift of a light object was preceded by a heavy relative to a light object. This relationship was not significantly altered when lifting with gloves, suggesting that the addition of gloves did not change sensorimotor memory effects. We conclude that FAI fibers may be important for the online force scaling but not for the buildup of a sensorimotor memory.