Sensorimotor Memory Research Articles

The cerebellum acts as the analog to the medial temporal lobe for sensorimotor memory

The cerebellum is critical for sensorimotor learning. The specific contribution that it makes, however, remains unclear. Inspired by the classic finding that for declarative memories, medial temporal lobe (MTL) structures provide a gateway to the formation of long-term memory but are not required for short-term memory, we hypothesized that for sensorimotor memories, the cerebellum may play an analogous role. Here, we studied the sensorimotor learning of individuals with severe ataxia from cerebellar degeneration. We dissected the memories they formed during sensorimotor learning into a short-term temporally-volatile component, that decays rapidly with a time constant of just 15 to 20 s and thus cannot lead to long-term retention, and a longer-term temporally-persistent component that is stable for 60 s or more and leads to long-term retention. Remarkably, we find that these individuals display dramatically reduced levels of temporally-persistent sensorimotor memory, despite spared and even elevated levels of temporally-volatile sensorimotor memory. In particular, we find both impairment that systematically worsens with memory window duration over shorter memory windows (<12 s) and near-complete impairment of memory maintenance over longer memory windows (>25 s). This dissociation uncovers a unique role for the cerebellum as a gateway for the formation of long-term but not short-term sensorimotor memories, mirroring the role of the MTL for declarative memories. It thus reveals the existence of distinct neural substrates for short-term and long-term sensorimotor memory, and it explains both the trial-to-trial differences identified in this study and long-standing study-to-study differences in the effects of cerebellar damage on sensorimotor learning ability.

Repeated context-specific actions disrupt feedforward adjustments in motor commands in younger and older adults.

The flexibility of the motor system to adjust a planned action before or during the execution of the movement in response to sensory information is critical for preventing errors in motor control. As individuals age, this function declines, leading to an increased incidence of motor errors. Although sensory processing and cognitive decline are known contributors to this impairment, here, we test the hypothesis that repetition of context-specific planned actions interferes with the adjustment of feedforward motor commands. Younger and older participants were instructed to grasp and lift a T-shaped object with a concealed, off-sided center of mass and minimize its roll through anticipatory force control, relying predominantly on predictive model-driven planning (i.e., sensorimotor memories) developed through repeated lifts. We selectively manipulate the number of trial repeats with the center of mass on one side before switching it to the other side of the T-shaped object. The results showed that increasing the number of repetitions improved performance in manipulating an object with a given center of mass but led to increased errors when the object's center of mass was switched. This deleterious effect of repetition on feedforward motor adjustment was observed in younger and older adults. Critically, we show these effects on an internal model-driven motor planning task that relies predominantly on sensorimotor memory, with no differences in sensory inputs from the repetition manipulation. The findings indicate that feedforward motor adjustments are hampered by repetitive stereotyped planning and execution of motor behavior.NEW & NOTEWORTHY Adjusting planned actions in response to sensory stimuli degrades with age contributing to increased incidence of errors ranging from clumsy spills to catastrophic falls. Multiple factors likely contribute to age-related motor inflexibility, including sensory- and cognition-supporting system declines. Here, we present compelling evidence for repetition to disrupt feedforward adjusting of motor commands in younger and older adults, which suggests increases in stereotypy as a deleterious potentiator of motor control errors.

Exploring Saliency for Learning Sensory-Motor Contingencies in Loco-Manipulation Tasks

The objective of this paper is to propose a framework for a robot to learn multiple Sensory-Motor Contingencies from human demonstrations and reproduce them. Sensory-Motor Contingencies are a concept that describes intelligent behavior of animals and humans in relation to their environment. They have been used to design control and planning algorithms for robots capable of interacting and adapting autonomously. However, enabling a robot to autonomously develop Sensory-Motor Contingencies is challenging due to the complexity of action and perception signals. This framework leverages tools from Learning from Demonstrations to have the robot memorize various sensory phases and corresponding motor actions through an attention mechanism. This generates a metric in the perception space, used by the robot to determine which sensory-motor memory is contingent to the current context. The robot generalizes the memorized actions to adapt them to the present perception. This process creates a discrete lattice of continuous Sensory-Motor Contingencies that can control a robot in loco-manipulation tasks. Experiments on a 7-dof collaborative robotic arm with a gripper, and on a mobile manipulator demonstrate the functionality and versatility of the framework.

Revealing hidden sensorimotor memories in mice with AD‐relevant pathology

AbstractBackgroundMemories must be accessible for them to be useful. Alzheimer’s disease (AD) is a progressive form of dementia in which cognitive capacities slowly deteriorate due to underlying neurodegeneration. Interestingly, anecdotal observations have demonstrated that Alzheimer’s patients can exhibit cognitive fluctuations during all stages of the disease. In particular, it is thought that contextual factors are critical for unlocking these hidden memories. To date, however, exploration of the neural basis of cognitive fluctuations has been hampered due to the lack of a behavioral approach in mouse models to dissociate memories from contextual performance.MethodOur previous work demonstrated that interleaving ‘reinforced’ trials with trials without reinforcement (‘probe’ trials) in an auditory go/no‐go discrimination task, allows us to distinguish between acquired sensorimotor memories and their contextual expression. Here, we used this approach, together with two‐photon calcium imaging on behaving AD‐relevant mice (APP/PS1+), to determine whether amyloid accumulation impacts underlying sensorimotor memories (measured using ‘probe’ trials) and/or contextual‐performance (measured using ‘reinforced’ trials) in an age dependent manner.ResultImportantly, peripheral auditory function, measured using the threshold for detecting an auditory brainstem response, was similar between WT and APP/PS1+ mice. We found that while contextual‐performance is significantly impaired in young adult APP/PS1+ mice compared to age‐matched controls, these animals show only minor impairments in the underlying sensorimotor memories. However, middle aged APP/PS1+ mice show deficits in both domains. The impairment found in the young adults was accompanied by a reduction in stimulus selectivity and behavioral encoding in the auditory cortex of APP/PS1+ mice that that can be partially restored in probe trials. Ongoing analyses aim to identify whether this impairment is cortex‐wide or is concentrated near Aβ plaques. Finally, these effects were recapitulated by using a reinforcement learning model that accounts for changes in contextual signals. The main network model parameters affected between the control and the APP/PS1+ mice were those governing contextual scaling and behavioral inhibition.ConclusionThese results suggest that Aβ deposition impacts circuits involved in contextual computations before those involved in acquiring knowledge and that neural circuit interventions, such as modulating inhibition, may hold promise to reveal hidden memories.

Sensorimotor memories influence movement kinematics but not associated tactile processing

When interacting with objects, we often rely on visual information. However, vision is not always the most reliable sense for determining relevant object properties. For example, when the mass distribution of an object cannot be inferred visually, humans may rely on predictions about the object’s dynamics. Such predictions may not only influence motor behavior but also associated processing of movement-related afferent information, leading to reduced tactile sensitivity during movement. We examined whether predictions based on sensorimotor memories influence grasping kinematics and associated tactile processing. Participants lifted an object of unknown mass distribution and reported whether they detected a tactile stimulus on their grasping hand during the lift. In Experiment 1, the mass distribution could change from trial to trial, whereas in Experiment 2, we intermingled longer with shorter parts of constant and variable mass distributions, while also providing implicit or explicit information about the trial structure. In both experiments, participants grasped the object by predictively choosing contact points that would compensate the mass distribution experienced in the previous trial. Tactile suppression during movement, however, was invariant across conditions. These results suggest that predictions based on sensorimotor memories can influence movement kinematics but not associated tactile perception.

Contribution of implicit memory to adaptation of movement extent during reaching against unpredictable spring-like loads: insensitivity to intentional suppression of kinematic performance.

We examined the extent to which intentionally underperforming a goal-directed reaching task impacts how memories of recent performance contribute to sensorimotor adaptation. Healthy human subjects performed computerized cognition testing and an assessment of sensorimotor adaptation, wherein they grasped the handle of a horizontal planar robot while making goal-directed out-and-back reaching movements. The robot exerted forces that resisted hand motion with a spring-like load that changed unpredictably between movements. The robotic test assessed how implicit and explicit memories of sensorimotor performance contribute to the compensation for the unpredictable changes in the hand-held load. After each movement, subjects were to recall and report how far the hand moved on the previous trial (peak extent of the out-and-back movement). Subjects performed the tests under two counter-balanced conditions: one where they performed with their best effort, and one where they intentionally sabotaged (i.e., suppressed) kinematic performance. Results from the computerized cognition tests confirmed that subjects understood and complied with task instructions. When suppressing performance during the robotic assessment, subjects demonstrated marked changes in reach precision, time to capture the target, and reaction time. We fit a set of limited memory models to the data to identify how subjects used implicit and explicit memories of recent performance to compensate for the changing loads. In both sessions, subjects used implicit, but not explicit, memories from the most recent trial to adapt reaches to unpredictable spring-like loads. Subjects did not "give up" on large errors, nor did they discount small errors deemed "good enough". Although subjects clearly suppressed kinematic performance (response timing, movement variability, and self-reporting of reach error), the relative contributions of sensorimotor memories to trial-by-trial variations in task performance did not differ significantly between the two testing conditions. We conclude that intentional performance suppression had minimal impact on how implicit sensorimotor memories contribute to adaptation of unpredictable mechanical loads applied to the hand.

Visual information following object grasp supports digit position variability and swift anticipatory force control.

Anticipatory force control underlying dexterous manipulation has historically been understood to rely on visual object properties and on sensorimotor memories associated with previous experiences with similar objects. However, it is becoming increasingly recognized that anticipatory force control also relies on how an object is grasped. Experiments that allow unconstrained grasp contact points when preventing tilting an object with an off-centered mass show trial-to-trial variations in digit position and subsequent scaling of lift forces, all before feedback of object properties becomes available. Here, we manipulated the availability of visual information before reach onset and after grasp contact (with no vision during the reach) to determine the contribution and timing of visual information processing to the scaling of fingertip forces during dexterous manipulation at flexible contact points. Results showed that anticipatory force control was similarly successful, quantified as an appropriate compensatory torque at lift onset that counters the external torque of an object with a left and right center of mass, irrespective of the timing and availability of visual information. However, the way in which anticipatory force control was achieved varied depending on the availability of visual information. Visual information following grasp contact was associated with greater use of an asymmetric thumb and index finger grasp configuration to generate a compensatory torque and digit position variability, together with faster fingertip force scaling and sensorimotor learning. This result supports the hypothesis that visual information at a critical and functionally relevant time point following grasp contact supports variable and swift digit-based force control for dexterous object manipulation.NEW & NOTEWORTHY Humans excel in dexterous object manipulation by precisely coordinating grasp points and fingertip forces, highlighted in scenarios requiring countering object torques in advance, e.g., lifting a teacup without spilling will demand a unique digit force pattern based on the grip configuration at lift onset. Here, we show that visual information following grasp contact, a critical and functionally relevant time point, supports digit position variability and swift anticipatory force control to achieve a dexterous motor goal.

Sensorimotor control of object manipulation following middle cerebral artery (MCA) stroke

Methods for assessing the loss of hand function post-stroke examine limited aspects of motor performance and are not sensitive to subtle changes that can cause deficits in everyday object manipulation tasks. Efficiently lifting an object entails a prediction of required forces based on intrinsic features of the object (sensorimotor integration), short-term updates in the forces required to lift objects that are poorly predicted (sensorimotor memory), as well as the ability to modulate distal fingertip forces, which are not measured by existing assessment tools used in clinics for both diagnostic and rehabilitative purposes. The presented research examined these three components of skilled object manipulation in 60 chronic, unilateral middle cerebral artery stroke participants. Performance was compared to age-matched control participants, and linear regressions were used to predict performance based on clinical scores. Most post-stroke participants performed below control levels in at least one of the tasks. Post-stroke participants presented with combinations of deficits in each of the tasks performed, regardless of the hemisphere damaged by the stroke. Surprisingly, the ability to modulate distal forces was impaired in those patients with damage ipsilateral (right hemisphere) to the hand being used. Sensorimotor integration was also impaired in patients with right hemisphere damage, though they performed at control levels in later lifts, whereas left-hemisphere-damaged patients did not. Lastly, during a task requiring sensorimotor memory, neither patient group performed outside of control ranges on initial lifts, with patients with right hemisphere damage showing impaired performance in later lifts suggesting they were unable to learn the mapping novel mapping of color and mass of the objects. The presented research demonstrates unilateral MCA stroke patients can have deficits in one or more components required for the successful manipulation of hand-held objects and that skillful object lifting requires intact bilateral systems. Further, this information may be used in future studies to aid efforts that target rehabilitation regimens to a stroke survivor's specific pattern of deficits.

Transfer of weight information depends differently on used hand and handedness for perception and action.

When lifting an object sequentially with the two hands, information about object weight can be transferred from one hand to the other. This information can be used to predictively scale fingertip forces and to form a perceptual estimation about the object's weight. This study investigated how weight information can be transferred between the two hands and how this depends on the used hand and handedness of the participant. Right- and left-handed participants lifted light and heavy objects with the right or left hand in a pseudorandomized order and estimated the object's weight. Results showed that predictive force scaling depended on the previously lifted object, with higher force rates if a previous object was heavy. This known effect of sensorimotor memory was mostly independent of the used hand and handedness, indicating that weight information could be transferred across hands for fingertip force scaling. Furthermore, a perceptual bias that depended on the previous lifted object was found, with lower weight estimations when the previous object was heavy compared to light. While this bias was found for both light and heavy objects in right-handers, it was only observed for light objects in left-handers. Notably, in contrast to the results on force scaling, this effect was not transferred across hands. These findings indicate that the transfer of weight information depends differently on the used hand and handedness for perceptual estimations and predictive force scaling.

The effects of explicit and implicit information on modulation of corticospinal excitability during hand-object interactions

Fingertip force scaling during hand-object interactions typically relies on visual information about the object and sensorimotor memories from previous object interactions. Here, we investigated whether contextual information, that is not explicitly linked to the intrinsic object properties (e.g., size or weight) but that is informative for motor control requirements, can mediate force scaling. For this, we relied on two separate behavioral tasks during which we applied transcranial magnetic stimulation (TMS) to probe corticospinal excitability (CSE), as a window onto the primary motor cortex role in controlling fingertip forces. In experiment 1, participants performed a force tracking task, where we manipulated available implicit and explicit visual information. That is, either the force target was fully visible, or only the force error was displayed as a deviation from a horizontal line. We found that participants’ performance was better when the force target was fully visible, i.e., when they had explicit access to predictive information. However, we did not find differences in CSE modulation based on the type of visual information. On the other hand, CSE was modulated by the change in muscle contraction, i.e., contraction vs. relaxation and fast vs. slow changes. In sum, these findings indicate that CSE only reflects the ongoing motor command. In experiment 2, other participants performed a sequential object lifting task of visually identical objects that were differently weighted, in a seemingly random order. Within this task, we hid short series of incrementally increasing object weights. This allowed us to investigate whether participants would scale their forces for specific object weights based on the previously lifted object (i.e., sensorimotor effect) or based on the implicit information about the hidden series of incrementally increasing weights (i.e., extrapolation beyond sensorimotor effects). Results showed that participants did not extrapolate fingertip forces based on the hidden series but scaled their forces solely on the previously lifted object. Unsurprisingly, CSE was not modulated differently when lifting series of random weights versus series of increasing weights. Altogether, these results in two different grasping tasks suggest that CSE encodes ongoing motor components but not sensorimotor cues that are hidden within contextual information.

Effects of brain-derived neurotrophic factor (BDNF) on the Schizophrenia model of animals

BackgroundSchizophrenia（SCZ）is a common clinically chronic psychiatric disease, and there have no effective specific therapeutic drugs in clinical practice currently. Studies have shown that the expression level of brain-derived neurotrophic factor (BDNF) in schizophrenics has decreased, so the expression level of BDNF has always been one of the evaluation indicators of SCZ. The neurotrophic factor hypothesis believes that increase or decrease of the expression level of BDNF may be one of the pathophysiological basis of SCZ. MethodsIn this study, schizophrenic mice model with MK-801-induced glutamate dysfunction was established, and two doses of BDNF were administered to schizophrenic mice by intranasal administration. The four groups of mice: Control group, Model group, BDNF-20, BDNF-100 performed a series of behavioral tests to explore the effects of BDNF on sensory motor gating, anxiety, depression, social interaction, spontaneous activity, and memory in schizophrenic mice. Transcriptome sequencing of the BDNF high group and Model group in prefrontal cortex and hippocampus, using Metascape for gene function annotation and enrichment pathway analysis, to obtain BDNF transcription regulation information, understand the molecular mechanism of BDNF in SCZ further. Subsequently，immunofluorescence detected the effects of BDNF on neurons and glial cells in the prefrontal cortex and hippocampus. ConclusionThe results show that BDNF can improve the behavior of SCZ by regulating the construction of the nervous system, affecting the growth and distribution of neurons and glial cells, and changing inflammation and apoptosis in the brain.

Object-centered sensorimotor bias of torque control in the chronic stage following stroke

When lifting objects whose center of mass (CoM) are not centered below the handle one must compensate for arising external torques already at lift-off to avoid object tilt. Previous studies showed that finger force scaling during object lifting may be impaired at both hands following stroke. However, torque control in object manipulation has not yet been studied in patients with stroke. In this pilot study, thirteen patients with chronic stage left hemispheric stroke (SL), nine patients with right hemispheric stroke (SR) and hand-matched controls had to grasp and lift an object with the fingertips of their ipsilesional hand at a handle while preventing object tilt. Object CoM and therewith the external torque was varied by either relocating a covert weight or the handle. The compensatory torque at lift-off (Tcom) is the sum of the torque resulting from (1) grip force being produced at different vertical finger positions (∆CoP × GF) and (2) different vertical load forces on both sides of the handle (∆Fy × w/2). When having to rely on sensorimotor memories, ∆CoP × GF was elevated when the object CoM was on the ipsilesional-, but decreased when CoM was on the contralesional side in SL, whereas ∆Fy × w/2 was biased in the opposite direction, resulting in normal Tcom. SR patients applied a smaller ∆CoP × GF when the CoM was on the contralesional side. Torques were not altered when geometric cues were available. Our findings provide evidence for an object-centered spatial bias of manual sensorimotor torque control with the ipsilesional hand following stroke reminiscent of premotor neglect. Both intact finger force-to-position coordination and visuomotor control may compensate for the spatial sensorimotor bias in most stroke patients. Future studies will have to confirm the found bias and evaluate the association with premotor neglect.

Chronic, acute and protocol-dependent effects of exercise on psycho-physiological health during long-term isolation and confinement

Exercise could prevent physical and psychological deteriorations, especially during pandemic times of lock-down scenarios and social isolation. But to meet both, the common exercise protocols require optimization based on holistic investigations and with respect to underlying processes. This study aimed to explore individual chronic and acute effects of continuous and interval running exercise on physical and cognitive performance, mood, and affect and underlying neurophysiological factors during a terrestrial simulated space mission. Six volunteers (three females) were isolated for 120 days. Accompanying exercise training consisted of a continuous and interval running protocol in a cross-over design. Incremental stage tests on a treadmill were done frequently to test physical performance. Actigraphy was used to monitor physical activity level. Cognitive performance, mood (MoodMeter®), affect (PANAS), brain-derived neurotrophic factor (BDNF), insulin-like growth factor 1 (IGF-1), vascular-endothelial growth factor (VEGF), and saliva cortisol were investigated prior to, four times during, and after isolation, pre- and post-exercise on two separate days, respectively. As a chronic effect, physical performance increased (and IGF-1 tended) in the course of isolation and training until the end of isolation. Subjective mood and affect state, as well as cognitive performance, basal BDNF and VEGF levels, were well-preserved across the intervention. No acute effects of exercise were detected, besides slower reaction time after exercise in two out of nine cognitive tests, testing sensorimotor speed and memory of complex figures. Consistently higher basal IGF-1 concentrations and faster reaction time in the psychomotor vigilance test were found for the continuous compared to the interval running protocol. The results suggest that 120 days of isolation and confinement can be undergone without cognitive and mental deteriorations. Regular, individual aerobic running training supporting physical fitness is hypothesized to play an important role in this regard. Continuous running exercise seems to trigger higher IGF-1 levels and vigilance compared to interval running. Systematic and prolonged investigations and larger sample size are required to follow up on exercise-protocol specific differences in order to optimize the exercise intervention for long-term psycho-physiological health and well-being.

The role of motor memory dynamics in structuring bodily self-consciousness

Bodily self-consciousness has been considered a sensorimotor root of self-consciousness. If this is the case, how does sensorimotor memory, which is important for the prediction of sensory consequences of volitional actions, influence awareness of bodily self-consciousness? This question is essential for understanding the effective acquisition and recovery of self-consciousness following its impairment, but it has remained unexamined. Here, we investigated how body ownership and agency recovered following body schema distortion in a virtual reality environment along with two kinds of motor memories: memories that were rapidly updated and memories that were gradually updated. We found that, although agency and body ownership recovered in parallel, the recovery of body ownership was predicted by fast memories and that of agency was predicted by slow memories. Thus, the bodily self was represented in multiple motor memories with different dynamics. This finding demystifies the controversy about the causal relationship between body ownership and agency.

Brain functional networks analysis of five fingers grasping in virtual reality environment.

This study investigated the effects of different center of mass (COM) of the grasping device and visual time-delay on the information interaction between brain regions during five-finger grasping process. Nine healthy right-handed subjects used five fingers to grasp a special device in a virtual reality (VR) environment. Two independent variables were set in the experiment: the COM of the grasping device and the visual delay time. Place a 50 g mass randomly at five different directions of the grasping device base. The three levels of visual delay time appear randomly. The kinematics and dynamics and electroencephalogram (EEG) signals were recorded during the experiment. The brain network was constructed based on multiplex horizontal visibility graph (MHVG). Interlayer mutual information (MI) and phase locking value (PLV) were calculated to quantify the network, while clustering coefficient (C), shortest path length (L) and overall network efficiency (E) are selected to quantify the network characteristic. Statistical results show that when the mass is located in the radial side, during the load phase of grasping, the C and E is significantly higher than that in the proximal, ulnar and medial side, and L was significantly lower than that in the proximal and radial side. This shows that when grasping an object with a COM bias on the radial side, the process of brain feedforward control has higher level of information interaction and ability and it can build stronger sensorimotor memory. It is also found that the brain network features of theta, beta and gamma bands of EEG are positively correlated, especially between beta and gamma bands, which suggests there is a coupling relationship between different bands in information processing and transmission.Clinical Relevance- This study explains the neural mechanism of grasping control from the topological structure of the whole brain network level and the informatics.

A subcortical network for implicit visuo-spatial attention: Implications for Parkinson's Disease

Recent studies in humans and animal models suggest a primary role of the basal ganglia in the extraction of stimulus-value regularities, then exploited to orient attentional shift and build up sensorimotor memories. The tail of the caudate and the posterior putamen both receive early visual input from the superficial layers of the superior colliculus, thus forming a closed-loop. We portend that the functional value of this circuit is to manage the selection of visual stimuli in a rapid and automatic way, once sensory–motor associations are formed and stored in the posterior striatum. In Parkinson's Disease, the nigrostriatal dopamine depletion starts and tends to be more pronounced in the posterior putamen. Thus, at least some aspect of the visuospatial attention deficits observed since the early stages of the disease could be the behavioral consequences of a cognitive system that has lost the ability to translate high-level processing in stable sensorimotor memories.

How long is the interval over which trial-to-trial effects on Fitts' Law task can operate?

Fitts' Law is a well-studied principle in psychology which holds that movement time (MT) varies with the size and distance of a target across a wide range of tasks. In a recent study, the authors demonstrated that performance on a current trial in a Fitts' Law paradigm is affected by what happens during the previous trial (Tang et al. in Psychon Bull Rev 25(5):1833-1839, 2018). The aim of the present study was to explore how long this trial-to-trial transfer might last and whether or not the transfer would occur between the left and right hands. A series of experiments was carried out using discrete trials, a paradigm in which the current authors and others have previously established that Fitts' Law operates (Fitts and Peterson in J Exp Psychol 67(2):103-112, 1964; Tang et al. 2018). Three inter-trial intervals (3s, 4s, and 5s) were used in separate testing sessions, the order of which was counterbalanced across participants. In addition, trial-to-trial transfer was tested within a single hand and between hands. The results demonstrate that transfer from one trial to the next could bridge 4s when either the right or the left hand was used and would disappear by 5s. Moreover, the effect transferred between the two hands. The endpoint accuracy of the current trial was not affected by the previous trial. These findings suggest that the trial-to-trial effect reduces over time and that the transfer of sensorimotor memory or the task set is independent of the particular hand used.

Task Errors Drive Memories That Improve Sensorimotor Adaptation.

Traditional views of sensorimotor adaptation (i.e., adaptation of movements to perturbed sensory feedback) emphasize the role of automatic, implicit correction of sensory prediction errors. However, latent memories formed during sensorimotor adaptation, manifest as improved relearning (e.g., savings), have recently been attributed to strategic corrections of task errors (failures to achieve task goals). To dissociate contributions of task errors and sensory prediction errors to latent sensorimotor memories, we perturbed target locations to remove or enforce task errors during learning and/or test, with male/female human participants. Adaptation improved after learning in all conditions where participants were permitted to correct task errors, and did not improve whenever we prevented correction of task errors. Thus, previous correction of task errors was both necessary and sufficient to improve adaptation. In contrast, a history of sensory prediction errors was neither sufficient nor obligatory for improved adaptation. Limiting movement preparation time showed that the latent memories driven by learning to correct task errors take at least two forms: a time-consuming but flexible component, and a rapidly expressible, inflexible component. The results provide strong support for the idea that movement corrections driven by a failure to successfully achieve movement goals underpin motor memories that manifest as savings. Such persistent memories are not exclusively mediated by time-consuming strategic processes but also comprise a rapidly expressible but inflexible component. The distinct characteristics of these putative processes suggest dissociable underlying mechanisms, and imply that identification of the neural basis for adaptation and savings will require methods that allow such dissociations.SIGNIFICANCE STATEMENT Latent motor memories formed during sensorimotor adaptation manifest as improved adaptation when sensorimotor perturbations are reencountered. Conflicting theories suggest that this "savings" is underpinned by different mechanisms, including a memory of successful actions, a memory of errors, or an aiming strategy to correct task errors. Here we show that learning to correct task errors is sufficient to show improved subsequent adaptation with respect to naive performance, even when tested in the absence of task errors. In contrast, a history of sensory prediction errors is neither sufficient nor obligatory for improved adaptation. Finally, we show that latent sensorimotor memories driven by task errors comprise at least two distinct components: a time-consuming, flexible component, and a rapidly expressible, inflexible component.

Visual cues, expectations, and sensorimotor memories in the prediction and perception of object dynamics during manipulation

When we grasp and lift novel objects, we rely on visual cues and sensorimotor memories to predictively scale our finger forces and exert compensatory torques according to object properties. Recently, it was shown that object appearance, previous force scaling errors, and previous torque compensation errors strongly impact our percept. However, the influence of visual geometric cues on the perception of object torques and weights in a grasp to lift task is poorly understood. Moreover, little is known about how visual cues, prior expectations, sensory feedback, and sensorimotor memories are integrated for anticipatory torque control and object perception. Here, 12 young and 12 elderly participants repeatedly grasped and lifted an object while trying to prevent object tilt. Before each trial, we randomly repositioned both the object handle, providing a geometric cue on the upcoming torque, as well as a hidden weight, adding an unforeseeable torque variation. Before lifting, subjects indicated their torque expectations, as well as reporting their experience of torque and weight after each lift. Mixed-effect multiple regression models showed that visual shape cues governed anticipatory torque compensation, whereas sensorimotor memories played less of a role. In contrast, the external torque and committed compensation errors at lift-off mainly determined how object torques and weight were perceived. The modest effect of handle position differed for torque and weight perception. Explicit torque expectations were also correlated with anticipatory torque compensation and torque perception. Our main findings generalized across both age groups. Our results suggest distinct weighting of inputs for action and perception according to reliability.

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.