Biology subjects

Flanagan, J. R.

Publications and source records attributed to Flanagan, J. R..

18 recordsLinked to original sources

bioRxiv2026

Adaptive integration of model-based and model-free strategies in human reinforcement learning of reachable space

Most skilled behaviour occurs within reachable space; however, how humans learn to reach around obstacles in this space remains almost entirely unexplored. Here, using a novel robotic maze task that captures the richness of naturalistic hand-object interaction, we show that humans adaptively integrate model-based and model-free reinforcement learning strategies to act in reachable space. Fitting hybrid models to reach trajectories revealed that participants shifted from model-based toward model-free strategies across learning. Specifically, model-free reliance increased with state familiarity and distance from the goal, and with exclusive haptic feedback. Across participants, greater model-free reliance was associated with faster movements, consistent with reduced planning demands. Critically, direct comparison with an analogous virtual navigation task revealed stronger model-free reliance in reachable space than in navigable space, demonstrating that the computational architecture governing spatial learning is shared across scales but calibrated to the costs and constraints of the specific effector system.

neuroscience↗

bioRxiv2026

Independence of Visuomotor Functions Engaged in Visual Pursuit and Rapid Responses to Reach Errors

When reaching to a foveated target, peripheral vision of the hand can be used to make rapid, automatic adjustments to the ongoing reach movement, with the feedback gain being sensitive to features of the task and environment. These rapid corrective responses are also observed when gaze is directed to a stationary gaze target located away from the reach target. In everyday contexts, reaching often occurs concurrently with other visual or visuomotor tasks, such as tracking a moving target. Yet it remains unclear whether engaging in such tasks affects the use of peripheral vision for hand guidance. Here, we compare rapid visuomotor corrective responses to visual perturbations during fixation and smooth pursuit, and test whether pursuit-related and reach-related visuomotor processes operate independently or compete for shared visual resources. Participants either fixated a stationary target or tracked a moving target while reaching toward a spatially dissociated reach target. During the reach, the visual representation of the hand was perturbed, requiring rapid corrective responses. We found that neither the onset nor the gain of reach corrections was modulated by gaze-task demands. Moreover, response gains were strongly correlated across tasks, indicating consistent individual response profiles that were independent of the gaze condition. Despite modest increases in position error and decreases in gain, participants largely sustained engagement with the visual tasks during target reaching. These findings demonstrate that smooth pursuit and reach-related visuomotor processing can operate in parallel without mutual interference, suggesting a functional independence between them. NEW & NOTEWORTHYIn everyday life, reaching to an object can occur while the eyes are engaged in competing visual tasks. We show that engaging in smooth pursuit eye movements does not disrupt rapid visuomotor corrections during reaching. The onset and gain of corrective responses following perturbation were unchanged by gaze-task demands and were consistent across individuals. These findings demonstrate that pursuit and reach-related visuomotor processes can operate in parallel, supporting functional independence between these systems.

neuroscience↗

bioRxiv2025

Gaze-related functions driving gaze anchoring in reaching

When reaching to a target, we typically direct our gaze to the target throughout the reach. If a secondary saccade target is presented during the reach, and we are instructed to shift our gaze to this target, the gaze shift is generally delayed until the reach target has been attained--a phenomenon known as gaze anchoring. Here, we compared gaze anchoring in human participants when reaching to a visual target versus a visual-haptic target providing force feedback upon contact. We also examined gaze anchoring in a bimanual context in which participants reached with their right hand and were instructed to both shift their gaze and move their left hand to the secondary target as soon as it appeared. We found that, during the reaching movement, gaze was anchored to the target for both visual and visual-haptic targets. In the visual-haptic condition, gaze appeared to be anchored during the initial directing phase of the reach during which peripheral vision directs the hand to the vicinity of the target. In the visual condition, gaze appeared to be anchored during both the directing phase and subsequent guiding phase during which central visual guides the hand. In two-handed reaching, gaze anchoring was observed but anchoring did not extend to the left hand, which started moving before the eyes. Overall, our findings indicate that the timing of eye and hand movements in object manipulation is linked to the function of target fixations. New & NoteworthyWhen reaching to a visual target, gaze is typically anchored to the target even when a competing saccade target appears. We show that anchoring also occurs for visual-haptic targets but is limited to the initial phase of the reach, likely because vision is not required to confirm target attainment. In contrast to gaze, anchoring is not observed for the non-reaching hand, which can begin moving to a competing target as soon as it appears.

neuroscience↗

bioRxiv2024

Adaptive Gaze and Hand Coordination while Manipulating and Monitoring the Environment in Parallel

Research on visually guided object manipulation has shown that participants fixate goal locations-such as objects to be grasped and locations where they are placed-prior to hand arrival, with gaze serving two primary functions: directing the hand (or object in hand) to the vicinity of the goal using peripheral vision and gaze related signals, and guiding the hand using central vision as it approaches the goal. However, in real world scenarios, manipulation tasks are often performed while concurrent monitoring of the environment, resulting in competition for gaze. Here we examined gaze-hand coordination under such conditions. Participants performed a manipulation task, that involved grasping balls and placing them at target locations, while concurrently monitoring a display to detect probabilistically occurring visual events, which required central vision. Participants managed gaze competition in two main ways. First, fixations allocated to the action task were brief and prioritized directing the hand towards the goal (object or target location); participants then relied on tactile feedback to complete the action (grasping or placing the object). When tactile feedback was reduced-by using a tool instead of the fingertips to perform the task-gaze additionally served the guiding function. Second, participant reduced gaze competition by exploiting temporal regularities of events in the monitoring task. Specifically, they adjusted both gaze allocation and hand movement timing to reduce the likelihood that action task fixations would coincide with visual events. These findings demonstrate how individuals flexibly integrate sensorimotor control with analysis of environmental statistics to manage competing visual demands. Significance StatementIn everyday behaviour, we often perform manual tasks while simultaneously monitoring the environment, creating competition for gaze. How the brain resolves this competition remains poorly understood. Using a novel paradigm combining an object manipulation task with visual event monitoring, we show that participants integrate knowledge of sensorimotor demands and temporal regularities in the monitoring task to manage gaze. Specifically, we found that participants preferentially allocated gaze to the action task when it is most critical for sensorimotor control and when the likelihood of a visual event was low. Additionally, participants adjusted their hand movement timing based on event statistics to reduce gaze competition. These findings reveal how the brain dynamically allocates gaze resources across competing sensorimotor and visual task demands.

neuroscience↗

bioRxiv2024

Individual variability in sensorimotor learning reflects trait-like neurobehavioral subject factors

Models of Human motor behaviour often emphasize the computations performed by the motor system during learning. Yet, there is an emerging consensus that the learning of even simple motor actions can be augmented by sophisticated cognitive strategies, which rely upon executive functions implemented throughout the cortex. These executive functions, in turn, have been linked to stable subject differences in intrinsic brain organization function, observable even during rest. Here we show, using behavioural studies in humans, that individual differences in the rate of sensorimotor adaptation are linked to differences in executive function, as assessed using the classic trail-making task. Secondly, using separate train and test functional MRI datasets, we show that specific patterns of resting-state functional connectivity between higher-order cognitive brain networks, which have been previously linked to executive function, subsequently predict more rapid learning during sensorimotor adaptation. Importantly, this relationship was unique to cognitive brain networks, as the functional connectivity between sensorimotor brain networks did not predict subsequent motor learning performance. Together, these findings suggest that individual differences in motor learning reflect, to a substantial degree, trait-like subject differences in cognitive brain network structure. This perspective invites broader consideration as to the origins of motor learning ability, and links motor performance to an expansive literature implicating the coordinated functioning of the default mode, ventral attention, and frontoparietal networks in flexible behavioral control.

neuroscience↗

bioRxiv2023

Whole-brain modular dynamics at rest predict sensorimotor learning performance

Predictive biomarkers of cognitive performance are informative about the neural mechanisms underlying cognitive phenomena, and have tremendous potential for the diagnosis and treatment of neuropathologies with cognitive symptoms. Among such biomarkers, the modularity (subnetwork composition) of whole-brain functional networks is especially promising, due to its longstanding theoretical foundations and recent success in predicting clinical outcomes. We used functional magnetic resonance imaging to identify whole-brain modules at rest, calculating metrics of their spatio-temporal dynamics before and after a sensorimotor learning task on which fast learning is widely believed to be supported by a cognitive strategy. We found that participants learning performance was predicted by the strength of dynamic modularity scores (clarity of subnetwork composition), the degree of coordination of modular reconfiguration, and the strength of recruitment and integration of networks derived during the task itself. Our findings identify these whole-brain metrics as promising biomarkers of cognition, with relevance to basic and clinical neuroscience.

neuroscience↗

bioRxiv2023

Reconfigurations of cortical manifold structure during reward-based motor learning

Adaptive motor behavior depends on the coordinated activity of multiple neural systems distributed across the brain. While the role of sensorimotor cortex in motor learning has been well-established, how higher-order brain systems interact with sensorimotor cortex to guide learning is less well understood. Using functional MRI, we examined human brain activity during a reward-based motor task where subjects learned to shape their hand trajectories through reinforcement feedback. We projected patterns of cortical and striatal functional connectivity onto a low-dimensional manifold space and examined how regions expanded and contracted along the manifold during learning. During early learning, we found that several sensorimotor areas in the Dorsal Attention Network exhibited increased covariance with areas of the salience/ventral attention network and reduced covariance with areas of the default mode network (DMN). During late learning, these effects reversed, with sensorimotor areas now exhibiting increased covariance with DMN areas. However, areas in posteromedial cortex showed the opposite pattern across learning phases, with its connectivity suggesting a role in coordinating activity across different networks over time. Our results establish the neural changes that support reward-based motor learning and identify distinct transitions in the functional coupling of sensorimotor to transmodal cortex when adapting behavior.

neuroscience↗

bioRxiv2023

The structural-functional neural architectures of implicit and explicit motor learning

Sensorimotor learning is supported by multiple competing processes that operate concurrently, making it a challenge to elucidate their neural underpinnings. Here, using human functional MRI, we identify three distinct axes of connectivity between the motor cortex and other brain regions during sensorimotor adaptation. These three axes uniquely correspond to subjects degree of implicit learning, performance errors and explicit strategy use, and involve different brain networks situated at increasing levels of the cortical hierarchy. We test the generalizability of these neural axes to a separate form of motor learning known to rely mainly on explicit processes, and show that it is only the Explicit neural axis, composed of higher-order areas in transmodal cortex, that predicts learning in this task. Together, our study uncovers multiple distinct patterns of functional connectivity with motor cortex during sensorimotor adaptation, the component processes that these patterns support, and how they generalize to other forms of motor learning.

neuroscience↗

bioRxiv2022

Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation

Sensorimotor learning is a dynamic, systems-level process that involves the combined action of multiple neural systems distributed across the brain. Although we understand a great deal about the specialized cortical systems that support specific components of action (such as reaching), we know less about how cortical systems function in a coordinated manner to facilitate adaptive behaviour. To address this gap in knowledge, our study measured human brain activity using functional MRI (fMRI) while participants performed a classic sensorimotor adaptation task, and used a manifold learning approach to describe how behavioural changes during adaptation relate to changes in the landscape of cortical activity. During early adaptation, we found that areas in parietal and premotor cortex exhibited significant contraction along the cortical manifold, which was associated with their increased covariance with regions in higher-order association cortex, including both the default mode and fronto-parietal networks. By contrast, during late adaptation, when visuomotor errors had been largely reduced, we observed a significant expansion of visual cortex along the cortical manifold, which was associated with its reduced covariance with association cortex and its increased intraconnectivity. Lastly, we found that individuals who learned more rapidly exhibited greater covariance between regions in the sensorimotor and association cortices during early adaptation. Together, these findings are consistent with a view that sensorimotor adaptation depends on changes in the integration and segregation of neural activity across more specialized regions of unimodal cortex with regions in association cortex implicated in higher-order processes. More generally, they lend support to an emerging line of evidence implicating regions of the default mode network in task-based performance.

neuroscience↗

bioRxiv2022

The influence of movement-related costs when searching to act and acting to search

Real world search behaviour often involves limb movements, either during search or following search. Here we investigated whether movement-related costs influence search behaviour in two kinds of search tasks. In our visual search tasks, participants made saccades to find a target object among distractors and then moved a cursor, controlled by the handle of a robotic manipulandum, to the target. In our manual search tasks, participants moved the cursor to perform the search, placing it onto objects to reveal their identity as either a target or a distractor. Across experiments, we manipulated either the effort or time costs associated with movement such that these costs varied across the search space. We varied effort by applying different resistive forces to the handle and we varied time costs by altering the speed of the cursor. Our analysis of cursor and eye movements during manual and visual search, respectively, showed that effort influenced manual search but did not influence visual search. In contrast, time costs influenced both visual and manual search. Our results demonstrate that, in addition to perceptual and cognitive factors, movement-related costs can also influence search behaviour. Public Significance StatementMany of the tasks we perform on a daily basis involve searching for targets. Numerous studies have investigated perceptual and cognitive factors that influence decisions about where to search. However, few studies have examined how search is influenced by movement-related costs associated with manual search (e.g., opening drawers to find a corkscrew) or acting on an object once it has been located (e.g., reaching for a particular bottle of wine once it has been spied in a rack). We show that movement effort and time costs associated with manual search, and time costs associated with moving after visual search, can influence decision-making about where to search over time.

neuroscience↗

bioRxiv2021

Neural Excursions from Low-Dimensional Manifold Structure Explain Intersubject Variation in Human Motor Learning

Humans vary greatly in their motor learning abilities, yet little is known about the neural mechanisms that underlie this variability. Recent neuroimaging and electrophysiological studies demonstrate that large-scale neural dynamics inhabit a low-dimensional subspace or manifold, and that learning is constrained by this intrinsic manifold architecture. Here we asked, using functional MRI, whether subject-level differences in neural excursion from manifold structure can explain differences in learning across participants. We had subjects perform a sensorimotor adaptation task in the MRI scanner on two consecutive days, allowing us to assess their learning performance across days, as well as continuously measure brain activity. We find that the overall neural excursion from manifold activity in both cognitive and sensorimotor brain networks is associated with differences in subjects patterns of learning and relearning across days. These findings suggest that off-manifold activity provides an index of the relative engagement of different neural systems during learning, and that intersubject differences in patterns of learning and relearning across days are related to reconfiguration processes in cognitive and sensorimotor networks during learning.

neuroscience↗

bioRxiv2021

Motor memories of object dynamics are categorically organized

The ability to predict the dynamics of objects, linking applied force to motion, underlies our capacity to perform many of the tasks we carry out on a daily basis. Thus, a fundamental question is how the dynamics of the myriad objects we interact with are organized in memory. Using a custom-built three-dimensional robotic interface that allowed us to simulate objects of varying appearance and weight, we examined how participants learned the weights of sets of objects that they repeatedly lifted. We find strong support for the novel hypothesis that motor memories of object dynamics are organized categorically, in terms of families, based on covariation in their visual and mechanical properties. A striking prediction of this hypothesis, supported by our findings and not predicted by standard associative map models, is that outlier objects with weights that deviate from the family-predicted weight will never be learned despite causing repeated lifting errors.

neuroscience↗

bioRxiv2020

Whole-brain dynamics of human sensorimotor adaptation

Humans vary greatly in their motor learning abilities, yet little is known about the neural processes that underlie this variability. We identified distinct profiles of human sensorimotor adaptation that emerged across two days of learning, linking these profiles to the dynamics of whole-brain functional networks early on the first day, when cognitive strategies toward sensorimotor adaptation are believed to be most prominent. During early learning, greater recruitment of a network of higher-order brain regions, involving prefrontal and anterior temporal cortex, was associated with faster learning. At the same time, greater integration of this cognitive network with a sensorimotor network was associated with slower learning, consistent with the notion that cognitive strategies toward adaptation operate in parallel with implicit learning processes of the sensorimotor system. On the second day, greater recruitment of a network that included the hippocampus was associated with faster re-learning, consistent with the notion that savings involves declarative memory systems. Together, these findings provide novel evidence for the role of higher-order brain systems in driving individual differences in adaptation.

neuroscience↗

bioRxiv2020

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.

neuroscience↗

bioRxiv2020

Gaze Behaviour Reveals Flexible Encoding of Competing Reach Goals Under Conditions of Target Uncertainty

In daily tasks, we are often confronted with competing potential targets and must select one to act on. It has been suggested that, prior to target selection, the human brain encodes the motor goals of multiple, potential targets. However, this view remains controversial and it has been argued that only a single motor goal is encoded, or that motor goals are only specified after target selection. To investigate this issue, we measured participants gaze behaviour while viewing two potential reach targets, one of which was cued after a preview period. We applied visuomotor rotations to dissociate each visual target location from its corresponding motor goal location; i.e., the location participants needed to aim their hand toward to bring the rotated cursor to the target. During the preview period, participants most often fixated both motor goals but also frequently fixated one, or neither, motor goal location. Further gaze analysis revealed that on trials in which both motor goals were fixated, both locations were held in memory simultaneously. These findings show that, at the level of single trials, the brain most often encodes multiple motor goals prior to target selection, but may also encode either one or no motor goals. This result may help reconcile a key debate concerning the specification of motor goals in cases of target uncertainty.

neuroscience↗

bioRxiv2020

Variation in error-based and reward-based human motor learning is related and associated with entorhinal volume

Error-based and reward-based processes are critical for motor learning, and are thought to be mediated via distinct neural pathways. However, recent behavioral work in humans suggests that both learning processes are supported by cognitive strategies and that these contribute to individual differences in motor learning ability. While it has been speculated that medial temporal lobe regions may support this strategic component to learning, direct evidence is lacking. Here we first show that faster and more complete learning during error-based visuomotor adaptation is associated with better learning during reward-based shaping of reaching movements. This result suggests that strategic processes, linked to faster and better learning, drive individual differences in both error-based and reward-based motor learning. We then show that right entorhinal cortex volume was larger in good learning individuals--classified across both motor learning tasks--compared to their poorer learning counterparts. This suggests that strategic processes underlying both error- and reward-based learning are linked to neuroanatomical differences in entorhinal cortex. Significance StatementWhile it is widely appreciated that humans vary greatly in their motor learning abilities, little is known about the processes and neuroanatomical bases that underlie these differences. Here, using a data-driven approach, we show that individual variability in error-based and reward-based motor learning is tightly linked, and related to the use of cognitive strategies. We further show that structural differences in entorhinal cortex predict this intersubject variability in motor learning, with larger entorhinal volumes being associated with better overall error-based and reward-based learning. Together, these findings provide support for the notion that the ability to recruit strategic processes underlies intersubject variability in both error-based and reward-based learning, which itself may be linked to structural differences in medial temporal regions.

neuroscience↗

bioRxiv2019

Motor planning modulates neural activity patterns in early human auditory cortex

It is well established that movement planning recruits motor-related cortical brain areas in preparation for the forthcoming action. Given that an integral component to the control of action is the processing of sensory information throughout movement, we predicted that movement planning might also modulate early sensory cortical areas, readying them for sensory processing during the unfolding action. To test this hypothesis, we performed two human functional MRI studies involving separate delayed movement tasks and focused on pre-movement neural activity in early auditory cortex, given its direct connections to the motor system and evidence that it is modulated by motor cortex during movement in rodents. We show that effector-specific information (i.e., movements of the left vs. right hand in Experiment 1, and movements of the hand vs. eye in Experiment 2) can be decoded, well before movement, from neural activity in early auditory cortex. We find that this motor-related information is represented in a separate subregion of auditory cortex than sensory-related information and is present even when movements are cued visually instead of auditorily. These findings suggest that action planning, in addition to preparing the motor system for movement, involves selectively modulating primary sensory areas based on the intended action.

neuroscience↗

bioRxiv2017

Fast and accurate edge orientation processing during object manipulation

Quickly and accurately extracting information about a touched objects orientation is a critical aspect of dexterous object manipulation. However, the speed and acuity of tactile edge orientation processing with respect to the fingertips as reported in previous perceptual studies appear inadequate in these respects. Here we directly establish the tactile systems capacity to process edge-orientation information during dexterous manipulation. Participants extracted tactile information about edge orientation very quickly, using it within 200 ms of first touching the object. Participants were also strikingly accurate. With edges spanning the entire fingertip, edge-orientation resolution was better than 3{degrees} in our object manipulation task, which is several times better than reported in previous perceptual studies. Performance remained impressive even with edges as short as 2 mm, consistent with our ability to precisely manipulate very small objects. Taken together, our results radically redefine the spatial processing capacity of the tactile system.

neuroscience↗