The archerfish uses motor adaptation in shooting to correct for changing physical conditions.

The archerfish is unique in its ability to hunt by shooting a jet of water from its mouth that hits insects situated above the water's surface. To aim accurately, the fish needs to overcome physical factors including changes in light refraction at the air-water interface. Nevertheless, archerfish can still hit the target with a high success rate under changing conditions. One possible explanation for this extraordinary ability is that it is learned by trial and error through a motor adaptation process. We tested this possibility by characterizing the ability of the archerfish to adapt to perturbations in the environment to make appropriate adjustments to its shots. We introduced a perturbing airflow above the water tank of the archerfish trained to shoot at a target. For each trial shot, we measured the error, i.e., the distance between the center of the target and the center of the water jet produced by the fish. Immediately after the airflow perturbation, there was an increase in shot error. Then, over the course of several trials, the error was reduced and eventually plateaued. After the removal of the perturbation, there was an aftereffect, where the error was in the opposite direction but washed out after several trials. These results indicate that archerfish can adapt to the airflow perturbation. Testing the fish with two opposite airflow directions indicated that adaptation took place within an egocentric frame of reference. These results thus suggest that the archerfish is capable of motor adaptation, as indicated by data showing that the fish produced motor commands that anticipated the perturbation.

Population-wide cerebellar growth models of children and adolescents.

In the past, the cerebellum has been best known for its crucial role in motor function. However, increasingly more findings highlight the importance of cerebellar contributions in cognitive functions and neurodevelopment. Using a total of 7240 neuroimaging scans from 4862 individuals, we describe and provide detailed, openly available models of cerebellar development in childhood and adolescence (age range: 6-17 years), an important time period for brain development and onset of neuropsychiatric disorders. Next to a traditionally used anatomical parcellation of the cerebellum, we generated growth models based on a recently proposed functional parcellation. In both, we find an anterior-posterior growth gradient mirroring the age-related improvements of underlying behavior and function, which is analogous to cerebral maturation patterns and offers evidence for directly related cerebello-cortical developmental trajectories. Finally, we illustrate how the current approach can be used to detect cerebellar abnormalities in clinical samples.

Boundary vector cells in the goldfish central telencephalon encode spatial information.

Navigation is one of the most fundamental cognitive skills for the survival of fish, the largest vertebrate class, and almost all other animal classes. Space encoding in single neurons is a critical component of the neural basis of navigation. To study this fundamental cognitive component in fish, we recorded the activity of neurons in the central area of the goldfish telencephalon while the fish were freely navigating in a quasi-2D water tank embedded in a 3D environment. We found spatially modulated neurons with firing patterns that gradually decreased with the distance of the fish from a boundary in each cell's preferred direction, resembling the boundary vector cells found in the mammalian subiculum. Many of these cells exhibited beta rhythm oscillations. This type of spatial representation in fish brains is unique among space-encoding cells in vertebrates and provides insights into spatial cognition in this lineage.

Prolonged Feedback Duration Does Not Affect Implicit Recalibration in a Visuomotor Rotation Task.

Visuomotor rotations are frequently used to study cognitive processes underlying motor adaptation. Explicit aiming strategies and implicit recalibration are two of these processes. A large body of literature indicates that both processes are in fact dissociable and mainly independent components that can be measured using different manipulations in visuomotor rotation tasks. Visual feedback is a crucial element in these tasks, and it therefore plays an important role when assessing explicit re-aiming and implicit recalibration. For instance, researchers have found timing of visual feedback to affect the contribution of implicit recalibration to learning: if feedback is shown only at the end of the movement (instead of continuously), implicit recalibration decreases. Similarly, participants show lower levels of implicit recalibration if visual feedback is presented with a delay (instead of immediately). We thus hypothesized that the duration of feedback availability might also play a role. The goal of this study was thus to investigate the effect of longer versus shorter feedback durations on implicit recalibration in human participants. To this end, we compared three feedback durations in a between-subject design: 200, 600, and 1200 ms. Using a large sample size, we found differences between groups to be quite small, to the point where most differences indicated statistical equivalence between group means. We therefore hypothesize that feedback duration, when only endpoint feedback is presented, has a negligible effect on implicit recalibration. We propose that future research investigate the effect of feedback duration on other parameters of adaptation, so as proprioceptive recalibration and explicit re-aiming.

Recognition of natural objects in the archerfish.

Recognition of individual objects and their categorization is a complex computational task. Nevertheless, visual systems can perform this task in a rapid and accurate manner. Humans and other animals can efficiently recognize objects despite countless variations in their projection on the retina due to different viewing angles, distance, illumination conditions and other parameters. To gain a better understanding of the recognition process in teleosts, we explored it in archerfish, a species that hunts by shooting a jet of water at aerial targets and thus can benefit from ecologically relevant recognition of natural objects. We found that archerfish not only can categorize objects into relevant classes but also can do so for novel objects, and additionally they can recognize an individual object presented under different conditions. To understand the mechanisms underlying this capability, we developed a computational model based on object features and a machine learning classifier. The analysis of the model revealed that a small number of features was sufficient for categorization, and the fish were more sensitive to object contours than textures. We tested these predictions in additional behavioral experiments and validated them. Our findings suggest the existence of a complex visual process in the archerfish visual system that enables object recognition and categorization.

Mini-review: The Role of the Cerebellum in Visuomotor Adaptation.

The incredible capability of the brain to quickly alter performance in response to ever-changing environment is rooted in the process of adaptation. The core aspect of adaptation is to fit an existing motor program to altered conditions. Adaptation to a visuomotor rotation or an external force has been well established as tools to study the mechanisms underlying sensorimotor adaptation. In this mini-review, we summarize recent findings from the field of visuomotor adaptation. We focus on the idea that the cerebellum plays a central role in the process of visuomotor adaptation and that interactions with cortical structures, in particular, the premotor cortex and the parietal cortex, may be crucial for this process. To this end, we cover a range of methodologies used in the literature that link cerebellar functions and visuomotor adaptation; behavioral studies in cerebellar lesion patients, neuroimaging and non-invasive stimulation approaches. The mini-review is organized as follows: first, we provide evidence that sensory prediction errors (SPE) in visuomotor adaptation rely on the cerebellum based on behavioral studies in cerebellar patients. Second, we summarize structural and functional imaging studies that provide insight into spatial localization as well as visuomotor adaptation dynamics in the cerebellum. Third, we discuss premotor - cerebellar interactions and how these may underlie visuomotor adaptation. And finally, we provide evidence from transcranial direct current and magnetic stimulation studies that link cerebellar activity, beyond correlational relationships, to visuomotor adaptation .

Individual differences in error-related frontal midline theta activity during visuomotor adaptation.

Post-feedback frontal midline EEG activity has been found to correlate with error magnitude during motor adaptation. However, the role of this neuronal activity remains to be elucidated. It has been hypothesized that post-feedback frontal midline activity may represent a prediction error, which in turn may be directly related to the adaptation process or to an unspecific orienting response. To address these hypotheses, we replicated a previous visuomotor adaptation experiment with very small perturbations, likely to invoke implicit adaptation, in a new group of 60 participants and combined it with EEG recordings. We found error-related peaks in the frontal midline electrodes in the time domain. However, these were best understood as modulations of frontal midline theta activity (FMT, 4-8 Hz). Trial-level differences in FMT correlated with error magnitude. This correlation was robust even for very small errors as well as in the absence of imposed perturbations, indicating that FMT does not depend on explicit or strategic re-aiming. Within participants, trial-level differences in FMT were not related to between-trial error corrections. Between participants, individual differences in FMT-error-sensitivity did not predict differences in adaptation rate. Taken together, these results imply that FMT does not drive implicit motor adaptation. Finally, individual differences in FMT-error-sensitivity negatively correlate to motor execution noise. This suggests that FMT reflects saliency: larger execution noise means a larger standard deviation of errors so that a fixed error magnitude is less salient. In conclusion, this study suggests that frontal midline theta activity represents a saliency signal and does not directly drive motor adaptation.

Measures of explicit and implicit in motor learning: what we know and what we don't.

Adaptation tasks are a key tool in characterizing the contribution of explicit and implicit processes to sensorimotor learning. However, different assumptions and ideas underlie methods used to measure these processes, leading to inconsistencies between studies. For instance, it is still unclear explicit and implicit combine additively. Cognitive studies of explicit and implicit processes show how non-additivity and bias in measurement can distort results. We argue that to understand explicit and implicit processes in visuomotor adaptation, we need a stronger characterization of the phenomenology and a richer set of models to test it on.

Methods matter: Your measures of explicit and implicit processes in visuomotor adaptation affect your results.

Visuomotor rotations are frequently used to study the different processes underlying motor adaptation. Explicit aiming strategies and implicit recalibration are two of these processes. Various methods, which differ in their underlying assumptions, have been used to dissociate the two processes. Direct methods, such as verbal reports, assume explicit knowledge to be verbalizable, where indirect methods, such as the exclusion, assume that explicit knowledge is controllable. The goal of this study was thus to directly compare verbal reporting with exclusion in two different conditions: during consistent reporting and during intermittent reporting. Our results show that our two conditions lead to a dissociation between the measures. In the consistent reporting group, all measures showed similar results. However, in the intermittent reporting group, verbal reporting showed more explicit re-aiming and less implicit adaptation than exclusion. Curiously, when exclusion was measured again, after the end of learning, the differences were no longer apparent. We suspect this may reflect selective decay in implicit adaptation, as has been reported previously. All told, our results clearly indicate that methods of measurement can affect the amount of explicit re-aiming and implicit adaptation that is measured. Since it has been previously shown that both explicit re-aiming and implicit adaptation have multiple components, discrepancies between these different methods may arise because different measures reflect different components.

Representation of edges, head direction, and swimming kinematics in the brain of freely-navigating fish.

Like most animals, the survival of fish depends on navigation in space. This capacity has been documented in behavioral studies that have revealed navigation strategies. However, little is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. We found that cells in the lateral pallium of the goldfish encode the edges of the environment, the fish head direction, the fish swimming speed, and the fish swimming velocity-vector. This study sheds light on how information related to navigation is represented in the brain of fish and addresses the fundamental question of the neural basis of navigation in this group of vertebrates.

A Revised Computational Neuroanatomy for Motor Control.

We discuss a new framework for understanding the structure of motor control. Our approach integrates existing models of motor control with the reality of hierarchical cortical processing and the parallel segregated loops that characterize cortical-subcortical connections. We also incorporate the recent claim that cortex functions via predictive representation and optimal information utilization. Our framework assumes that each cortical area engaged in motor control generates a predictive model of a different aspect of motor behavior. In maintaining these predictive models, each area interacts with a different part of the cerebellum and BG. These subcortical areas are thus engaged in domain-appropriate system identification and optimization. This refocuses the question of division of function among different cortical areas. What are the different aspects of motor behavior that are predictively modeled? We suggest that one fundamental division is between modeling of task and body whereas another is the model of state and action. Thus, we propose that the posterior parietal cortex, somatosensory cortex, premotor cortex, and motor cortex represent task state, body state, task action, and body action, respectively. In the second part of this review, we demonstrate how this division of labor can better account for many recent findings of movement encoding, especially in the premotor and posterior parietal cortices.

A Neuroanatomically Grounded Optimal Control Model of the Compensatory Eye Movement System in Mice.

We present a working model of the compensatory eye movement system in mice. We challenge the model with a data set of eye movements in mice (n =34) recorded in 4 different sinusoidal stimulus conditions with 36 different combinations of frequency (0.1-3.2 Hz) and amplitude (0.5-8°) in each condition. The conditions included vestibular stimulation in the dark (vestibular-ocular reflex, VOR), optokinetic stimulation (optokinetic reflex, OKR), and two combined visual/vestibular conditions (the visual-vestibular ocular reflex, vVOR, and visual suppression of the VOR, sVOR). The model successfully reproduced the eye movements in all conditions, except for minor failures to predict phase when gain was very low. Most importantly, it could explain the interaction of VOR and OKR when the two reflexes are activated simultaneously during vVOR stimulation. In addition to our own data, we also reproduced the behavior of the compensatory eye movement system found in the existing literature. These include its response to sum-of-sines stimuli, its response after lesions of the nucleus prepositus hypoglossi or the flocculus, characteristics of VOR adaptation, and characteristics of drift in the dark. Our model is based on ideas of state prediction and forward modeling that have been widely used in the study of motor control. However, it represents one of the first quantitative efforts to simulate the full range of behaviors of a specific system. The model has two separate processing loops, one for vestibular stimulation and one for visual stimulation. Importantly, state prediction in the visual processing loop depends on a forward model of residual retinal slip after vestibular processing. In addition, we hypothesize that adaptation in the system is primarily adaptation of this model. In other words, VOR adaptation happens primarily in the OKR loop.

Eye Movements during Visuomotor Adaptation Represent Only Part of the Explicit Learning.

Visuomotor rotations are learned through a combination of explicit strategy and implicit recalibration. However, measuring the relative contribution of each remains a challenge and the possibility of multiple explicit and implicit components complicates the issue. Recent interest has focused on the possibility that eye movements reflects explicit strategy. Here we compared eye movements during adaptation to two accepted measures of explicit learning: verbal report and the exclusion test. We found that while reporting, all subjects showed a match among all three measures. However, when subjects did not report their intention, the eye movements of some subjects suggested less explicit adaptation than what was measured in an exclusion test. Interestingly, subjects whose eye movements did match their exclusion could be clustered into the following two subgroups: fully implicit learners showing no evidence of explicit adaptation and explicit learners with little implicit adaptation. Subjects showing a mix of both explicit and implicit adaptation were also those where eye movements showed less explicit adaptation than did exclusion. Thus, our results support the idea of multiple components of explicit learning as only part of the explicit learning is reflected in the eye movements. Individual subjects may use explicit components that are reflected in the eyes or those that are not or some mixture of the two. Analysis of reaction times suggests that the explicit components reflected in the eye movements involve longer reaction times. This component, according to recent literature, may be related to mental rotation.

Intermanual transfer of visuomotor adaptation is related to awareness.

Previous studies compared the effects of gradual and sudden adaptation on intermanual transfer to find out whether transfer depends on awareness of the perturbation. Results from different groups were contradictory. Since results of our own study suggest that awareness depends on perturbation size, we hypothesize that awareness-related intermanual transfer will only appear after adaptation to a large, sudden perturbation but not after adaptation to a small sudden perturbation or a gradual perturbation, large or small. To confirm this, four groups (S30, G30, S75, G75) of subjects performed out-and-back reaching movements with their right arm. In a baseline block, they received veridical visual feedback of hand position. In the subsequent adaptation block, feedback was rotated by 30 deg (S30, G30) or 75 deg (S75, G75). This rotation was either introduced suddenly (S30, S75) or gradually in steps of 3 deg (G30, G75). After the adaptation block, subjects did an awareness test comprising exclusion and inclusion conditions. The experiment concluded with an intermanual transfer block, in which movements were performed with the left arm under rotated feedback, and a washout block again under veridical feedback. We used a hierarchical Bayesian model to estimate individual movement directions and group averages. The movement directions in different conditions were then used to calculate group and individual indexes of adaptation, awareness, unawareness, transfer and washout. Both awareness and transfer were larger in S75 than in other groups, while unawareness and washout were smaller in S75 than in other groups. Furthermore, the size of awareness indices correlated to intermanual transfer across subjects, even when transfer was normalized to final adaptation level. Thus, we show for the first time that the amount of intermanual transfer directly relates to the extent of awareness of the learned perturbation.

Long-range neural inhibition and stimulus competition in the archerfish optic tectum.

The archerfish, which is unique in its ability to hunt insects above the water level by shooting a jet of water at its prey, operates in a complex visual environment. The fish needs to quickly select one object from among many others. In animals other than the archerfish, long-range inhibition is considered to drive selection. As a result of long-range inhibition, a potential target outside a neuron's receptive field suppresses the activity elicited by another potential target within the receptive field. We tested whether a similar mechanism operates in the archerfish by recording the activity of neurons in the optic tectum while presenting a target stimulus inside the receptive field and a competing stimulus outside the receptive field. We held the features of the target constant while varying the size, speed, and distance of the competing stimulus. We found cells that exhibit long-range inhibition; i.e., inhibition that extends to a significant part of the entire visual field of the animal. The competing stimulus depressed the firing rate. In some neurons, this effect was dependent on the features of the competing stimulus. These findings suggest that long-range inhibition may play a crucial role in the target selection process in the archerfish.

Quantifying the social symptoms of autism using motion capture.

Autism Spectrum Disorder (ASD) is a remarkably heterogeneous condition where individuals exhibit a variety of symptoms at different levels of severity. Quantifying the severity of specific symptoms is difficult, because it either requires long assessments or observations of the ASD individual, or reliance on care-giver questionnaires, which can be subjective. Here we present a new technique for objectively quantifying the severity of several core social ASD symptoms using a motion capture system installed in a clinical exam room. We present several measures of child-clinician interaction, which include the distance between them, the proportion of time that the child approached or avoided the clinician, and the direction that the child faced in relation to the clinician. Together, these measures explained ~30% of the variance in ADOS scores, when using only ~5 minute segments of "free play" from the recorded ADOS assessments. These results demonstrate the utility of motion capture for aiding researchers and clinicians in the assessment of ASD social symptoms. Further development of this technology and appropriate motion capture measures for use in kindergartens and at home is likely to yield valuable information that will aid in quantifying the initial severity of core ASD symptoms and their change over time.

TMS motor mapping: Comparing the absolute reliability of digital reconstruction methods to the golden standard.

BACKGROUND: Changes in transcranial magnetic stimulation motor map parameters can be used to quantify plasticity in the human motor cortex. The golden standard uses a counting analysis of motor evoked potentials (MEPs) acquired with a predefined grid. Recently, digital reconstruction methods have been proposed, allowing MEPs to be acquired with a faster pseudorandom procedure. However, the reliability of these reconstruction methods has never been compared to the golden standard. OBJECTIVE: To compare the absolute reliability of the reconstruction methods with the golden standard. METHODS: In 21 healthy subjects, both grid and pseudorandom acquisition were performed twice on the first day and once on the second day. The standard error of measurement was calculated for the counting analysis and the digital reconstructions. RESULTS: The standard error of measurement was at least equal using digital reconstructions. CONCLUSION: Pseudorandom acquisition and digital reconstruction can be used in intervention studies without sacrificing reliability.

Individual Differences in Motor Noise and Adaptation Rate Are Optimally Related.

Individual variations in motor adaptation rate were recently shown to correlate with movement variability or "motor noise" in a forcefield adaptation task. However, this finding could not be replicated in a meta-analysis of adaptation experiments. Possibly, this inconsistency stems from noise being composed of distinct components that relate to adaptation rate in different ways. Indeed, previous modeling and electrophysiological studies have suggested that motor noise can be factored into planning noise, originating from the brain, and execution noise, stemming from the periphery. Were the motor system optimally tuned to these noise sources, planning noise would correlate positively with adaptation rate, and execution noise would correlate negatively with adaptation rate, a phenomenon familiar in Kalman filters. To test this prediction, we performed a visuomotor adaptation experiment in 69 subjects. Using a novel Bayesian fitting procedure, we succeeded in applying the well-established state-space model of adaptation to individual data. We found that adaptation rate correlates positively with planning noise (ß = 0.44; 95% HDI = [0.27 0.59]) and negatively with execution noise (ß = -0.39; 95% HDI = [-0.50 -0.30]). In addition, the steady-state Kalman gain calculated from planning and execution noise correlated positively with adaptation rate (r = 0.54; 95% HDI = [0.38 0.66]). These results suggest that motor adaptation is tuned to approximate optimal learning, consistent with the "optimal control" framework that has been used to explain motor control. Since motor adaptation is thought to be a largely cerebellar process, the results further suggest the sensitivity of the cerebellum to both planning noise and execution noise.

Cerebellar transcranial direct current stimulation interacts with BDNF Val66Met in motor learning.

BACKGROUND: Cerebellar transcranial direct current stimulation has been reported to enhance motor associative learning and motor adaptation, holding promise for clinical application in patients with movement disorders. However, behavioral benefits from cerebellar tDCS have been inconsistent. OBJECTIVE: Identifying determinants of treatment success is necessary. BDNF Val66Met is a candidate determinant, because the polymorphism is associated with motor skill learning and BDNF is thought to mediate tDCS effects. METHODS: We undertook two cerebellar tDCS studies in subjects genotyped for BDNF Val66Met. Subjects performed an eyeblink conditioning task and received sham, anodal or cathodal tDCS (N = 117, between-subjects design) or a vestibulo-ocular reflex adaptation task and received sham and anodal tDCS (N = 51 subjects, within-subjects design). Performance was quantified as a learning parameter from 0 to 100%. We investigated (1) the distribution of the learning parameter with mixture modeling presented as the mean (M), standard deviation (S) and proportion (P) of the groups, and (2) the role of BDNF Val66Met and cerebellar tDCS using linear regression presented as the regression coefficients (B) and odds ratios (OR) with equally-tailed intervals (ETIs). RESULTS: For the eyeblink conditioning task, we found distinct groups of learners (MLearner = 67.2%; SLearner = 14.7%; PLearner = 61.6%) and non-learners (MNon-learner = 14.2%; SNon-learner = 8.0%; PNon-learner = 38.4%). Carriers of the BDNF Val66Met polymorphism were more likely to be learners (OR = 2.7 [1.2 6.2]). Within the group of learners, anodal tDCS supported eyeblink conditioning in BDNF Val66Met non-carriers (B = 11.9% 95%ETI = [0.8 23.0]%), but not in carriers (B = 1.0% 95%ETI = [-10.2 12.1]%). For the vestibulo-ocular reflex adaptation task, we found no effect of BDNF Val66Met (B = -2.0% 95%ETI = [-8.7 4.7]%) or anodal tDCS in either carriers (B = 3.4% 95%ETI = [-3.2 9.5]%) or non-carriers (B = 0.6% 95%ETI = [-3.4 4.8]%). Finally, we performed additional saccade and visuomotor adaptation experiments (N = 72) to investigate the general role of BDNF Val66Met in cerebellum-dependent learning and found no difference between carriers and non-carriers for both saccade (B = 1.0% 95%ETI = [-8.6 10.6]%) and visuomotor adaptation (B = 2.7% 95%ETI = [-2.5 7.9]%). CONCLUSIONS: The specific role for BDNF Val66Met in eyeblink conditioning, but not vestibulo-ocular reflex adaptation, saccade adaptation or visuomotor adaptation could be related to dominance of the role of simple spike suppression of cerebellar Purkinje cells with a high baseline firing frequency in eyeblink conditioning. Susceptibility of non-carriers to anodal tDCS in eyeblink conditioning might be explained by a relatively larger effect of tDCS-induced subthreshold depolarization in this group, which might increase the spontaneous firing frequency up to the level of that of the carriers.