Reza Shadmehr's research while affiliated with Johns Hopkins Medicine and other places
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Publications (202)
Claiming agency is a prerequisite for taking responsibility: the brain must differentiate between the sensory events that are the erroneous consequences of our actions, and thus may be remedied if we change our behavior, and the many other events in our environment that consume our attention, but for which we have no means of influence. In the cere...
Significance
The information that one region of the brain transmits to another is usually viewed through the lens of firing rates. However, if the output neurons could vary the timing of their spikes, then, through synchronization, they would spotlight information that may be critical for control of behavior. Here we report that, in the cerebellum,...
During deliberation, as the brain considers its options, the neural activity representing the goodness of each option rises toward a threshold, and the choice is often dictated by the option for which the rise is fastest. Here we report a surprising correlate of these activities: saccade vigor. We engaged human subjects in a decision-making task in...
Sensorimotor learning is supported by at least two parallel systems: a strategic process that benefits from explicit knowledge, and an implicit process that adapts subconsciously. How do these systems interact? Does one system's contributions suppress the other, or do they operate independently? Here we illustrate that during reaching, implicit and...
Learning from error is often a slow process. In machine learning, the learning rate depends on a loss function that specifies a cost for error. Here, we hypothesized that during motor learning, error carries an implicit cost for the brain because the act of correcting for error consumes time and energy. Thus, if this implicit cost could be increase...
In science, as in life, one can only hope to both inform others, and be informed by them. The commentaries associated with our book Vigor have highlighted the many ways in which the theory that we proposed can be improved. For example, there are a myriad of factors that need to be considered in a fully encompassing objective function. The neural me...
The information that the brain transmits from one region to another is often viewed through the lens of firing rates. However, if the output neurons could vary the timing of their spikes with respect to each other, then through synchronization they could highlight information that may be critical for control of behavior. In the cerebellum, the comp...
Analysis of electrophysiological data from Purkinje cells (P-cells) of the cerebellum presents unique challenges to spike sorting. Complex spikes have waveforms that vary significantly from one event to the next, raising the problem of misidentification. Even when complex spikes are detected correctly, the simple spikes may belong to a different P-...
During foraging, animals decide how long to stay and harvest reward, and then abandon that site and travel with a certain speed to the next reward opportunity. One aspect of this behavior involves decision-making, while the other involves motor-control. A recent theory posits that control of decision-making and movements may be linked via a desire...
As you read this text, your eyes make saccades that guide your fovea from one word to the next. Accuracy of these movements require the brain to monitor and learn from visual errors. A current model suggests that learning is supported by two different adaptive processes, one fast (high error sensitivity, low retention), and the other slow (low erro...
During extended motor adaptation, learning appears to saturate despite persistence of residual errors. This adaptation limit is not fixed but varies with perturbation variance; when variance is high, residual errors become larger. These changes in total adaptation could relate to either implicit or explicit learning systems. Here, we found that whe...
Analysis of electrophysiological data from Purkinje cells (P-cells) of the cerebellum presents challenges for spike detection. Complex spikes have waveforms that vary significantly from one event to the next, raising the problem of misidentification. Even when complex spikes are detected correctly, the simple spikes may belong to a different P-cell...
Learning from error is often a slow process. To accelerate learning, previous motor adaptation studies have focused on explicit factors such as reward or punishment, but the results have been inconsistent. Here, we considered the idea that a movement error carries an implicit cost for the organism because the act of correcting for error consumes ti...
Learning from error is often a slow process. To accelerate learning, previous motor adaptation studies have focused on explicit factors such as reward or punishment, but the results have been inconsistent. Here, we considered the idea that a movement error carries an implicit cost for the organism because the act of correcting for error consumes ti...
Sensorimotor adaptation benefits from learning in two parallel systems: one that has access to explicit knowledge, and another that relies on implicit, unconscious correction. However, it is unclear how these systems interact: does enhancing one system’s contributions, for example through instruction, impair the other, or do they learn independentl...
Why do we run toward people we love, but only walk toward others? Why do people in New York seem to walk faster than other cities? Why do our eyes linger longer on things we value more? There is a link between how the brain assigns value to things, and how it controls our movements. This link is an ancient one, developed through shared neural circu...
The decision regarding which arm to use to perform a task reflects a complex process that can be influenced by many factors, including effort requirements of acquiring the goal. In this study, we considered a virtual reality environment in which people reached to a visual target in 3D space. To vary the cost of reaching, we altered the visual feedb...
The cerebellum resembles a feedforward, three-layer network of neurons in which the "hidden layer" consists of Purkinje cells (P-cells), and the output layer consists of deep cerebellar nucleus (DCN) neurons. In this analogy, the output of each DCN neuron is a prediction that is compared to the actual observation, resulting in an error signal that...
Artificial intelligence provides algorithms that describe how neural networks learn from error, but can the algorithms help uncover the neuronal wiring of the brain? Here, I consider the cerebellum, a major learning site that resembles a feedforward network of neurons. In the cerebellum, Purkinje cells (P-cells) organize in populations that converg...
Decisions are made based on the subjective value that the brain assigns to options. However, subjective value is a mathematical construct that cannot be measured directly, but rather inferred from choices. Recent results have demonstrated that reaction time, amplitude, and velocity of movements are modulated by reward, raising the possibility that...
In numerous paradigms, from fear conditioning to motor adaptation, memory exhibits a remarkable property: acquisition of a novel behavior followed by its extinction results in spontaneous recovery of the original behavior. A current model suggests that spontaneous recovery occurs because learning is supported by two different adaptive processes: on...
Anterograde interference refers to the negative impact of prior learning on the propensity for future learning. There is currently no consensus on whether this phenomenon is transient or long lasting, with studies pointing to an effect in the time scale of hours to days. These inconsistencies might be caused by the method employed to quantify perfo...
Every movement ends in a period of stillness. Current models assume that commands that hold the limb at a target location do not depend on the commands that moved the limb to that location. Here, we report a surprising relationship between movement and posture in primates: on a within-trial basis, the commands that hold the arm and finger at a targ...
In many forms of motor adaptation, performance approaches a limit at which point learning stops, despite the fact that errors remain. What causes this adaptation limit? Here we found that while reach adaptation exhibited an asymptotic limit, this limit was not fixed: when the variance of the perturbation decreased, the adaptation limit increased, a...
Decisions are made based on the subjective value that the brain assigns to options. However, subjective value is a mathematical construct that cannot be measured directly, but rather inferred from choices. Recent results have demonstrated that reaction time and velocity of movements are modulated by reward, raising the possibility that there is a l...
The common marmoset ( Callithrix Jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. H...
The common marmoset ( Callithrix Jacchus ) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory....
Movement vigor, defined as the reciprocal of the latency from availability of reward to its acquisition, changes with reward magnitude: movements exhibit shorter reaction time and increased velocity when they are directed toward more rewarding stimuli. This invigoration may be due to release of dopamine before movement onset, which has been shown t...
Anterograde interference refers to the negative impact of prior learning on the propensity for future learning. Previous work has shown that subsequent adaptation to two perturbations of opposing sign, A and B , impairs performance in B . Here, we aimed to unveil the mechanism at the basis of anterograde interference by tracking its impact as a fun...
To understand subjective evaluation of an option, various disciplines have quantified the interaction between reward and effort during decision making, producing an estimate of economic utility, namely the subjective ‘goodness’ of an option. However, variables that affect utility of an option also influence the vigor of movements toward that option...
A period of holding still follows every movement. It has been assumed that for the arm, moving and holding are functionally independent: movement is via an adaptive, feedback-dependent controller that generates commands to transport the arm, while holding is via setting of reflexes that produce a postural field at movement endpoint. This assumption...
Movements toward rewarding stimuli exhibit greater vigor, i.e., increased velocity and reduced reaction-times. This invigoration may be due to release of dopamine before movement onset. Dopamine release is strongly modulated by reward prediction error (RPE). Here, we generated an RPE event in the milliseconds before movement onset and tested whethe...
The capacity to move is essential for independence and declines with age. Limitations in mobility impact ~35% of adults over 70 and the majority of adults over 85. These limitations are highly associated with disability, dependency, and survival. More than 25-years ago the term "sarcopenia" was coined to highlight the age-related loss of muscle mas...
During foraging, animals decide how long to stay at a patch and harvest reward, and then, they move with certain vigor to another location. How does the brain decide when to leave, and how does it determine the speed of the ensuing movement? Here, we considered the possibility that both the decision-making and the motor control problems aimed to ma...
Rabbits can learn the biological analogue of a simple recursive function by relying only on the neurons of the cerebellum.
Neurons in various areas of the frontal and parietal lobes can be distinguished based on their preference for the direction of reach errors. Stimulation of these neurons corrects for those errors, uncovering a cortical system for adaptive motor control. Neurons in various areas of the frontal and parietal lobes can be distinguished based on their p...
A common aspect of individuality is our subjective preferences in evaluation of reward and effort. The neural circuits that evaluate these commodities influence circuits that control our movements, raising the possibility that vigor differences between individuals may also be a trait of individuality, reflecting a willingness to expend effort. In c...
The primary output cells of the cerebellar cortex, Purkinje cells, make kinematic predictions about ongoing movements via high-frequency simple spikes, but receive sensory error information about that movement via low-frequency complex spikes (CS). How is the vector space of sensory errors encoded by this low-frequency signal? Here we measured Purk...
Making a movement may be thought of as an economic decision in which one spends effort in order to acquire reward. Time discounts reward, which predicts that the magnitude of reward should affect movement vigor: we should move faster, spending greater effort, when there is greater reward at stake. Indeed, saccade peak velocities are greater and rea...
A recent policy change at Journal of Neuroscience (JN) has significantly increased editorial “desk rejections”, reducing the number of papers that are considered for publication. Survey results from 130 scientists suggested that the new policy may have had a particularly large impact on studies that focused on human behavioral techniques. To quanti...
Experience of a prediction error recruits multiple motor learning processes: some that learn strongly from error but have weak retention, some that learn weakly from error but exhibit strong retention. These processes are not generally observable, but are inferred from their collective influence on behavior. Is there a robust way to uncover the hid...
When we hold an object in our hand, the mass of the object alters the physics of our arm, changing the relationship between motor commands that our brain sends to our arm muscles and the resulting motion of our hand. If the object is unfamiliar to us, our first movement will exhibit an error, producing a trajectory that is different from the one we...
In generating a point to point movement, the brain does more than produce the transient commands needed to move the body part; it also produces the sustained commands that are needed to hold the body part at its destination. In the oculomotor system, these functions are mapped onto two distinct circuits: a pre-motor circuit that specializes in gene...
The integrity of the cerebellum is critical for accurate eye movements. Disruption of neurons in either the cerebellar oculomotor vermis or its projections to output nucleus of the cerebellum, the caudal fastigial nucleus (cFN), results in significant saccadic dysmetria (Goffart et al., 2004; Ohtsuka et al., 1994; Ritchie, 1976; Buzunov et al. 2013...
Given two rewarding stimuli, animals tend to choose the more rewarding (or less effortful) option. However, they also move faster toward that stimulus [1-5]. This suggests that reward and effort not only affect decision-making, they also influence motor control [6, 7]. How does the brain compute the effort requirements of a task? Here, we considere...
Unlabelled:
When we experience an error during a movement, we update our motor commands to partially correct for this error on the next trial. How does experience of error produce the improvement in the subsequent motor commands? During the course of an erroneous reaching movement, proprioceptive and visual sensory pathways not only sense the erro...
Previous research shows that human eye movements can serve as a valuable source of information about the structural elements of the oculomotor system and they also can open a window to the neural functions and cognitive mechanisms related to visual attention and perception. The research field of eye movement-driven biometrics explores the extractio...
Unlabelled:
During value-based decision-making, individuals consider the various options and select the one that provides the maximum subjective value. Although the brain integrates abstract information to compute and compare these values, the only behavioral outcome is often the decision itself. However, if the options are visual stimuli, during...
Execution of accurate eye movements depends critically on the cerebellum, suggesting that the major output neurons of the cerebellum, Purkinje cells, may predict motion of the eye. However, this encoding of action for rapid eye movements (saccades) has remained unclear: Purkinje cells show little consistent modulation with respect to saccade amplit...
Unlabelled:
In Parkinson's disease (PD), the human brain is capable of producing motor commands, but appears to require greater than normal subjective effort, particularly for the more-affected side. What is the nature of this subjective effort and can it be altered? We used an isometric task in which patients produced a goal force by engaging bot...
Cerebellar damage can profoundly impair human motor adaptation. For example, if reaching movements are perturbed abruptly, cerebellar damage impairs the ability to learn from the perturbation-induced errors. Interestingly, if the perturbation is imposed gradually over many trials, people with cerebellar damage may exhibit improved adaptation. Howev...
When movements are perturbed in adaptation tasks, humans and other animals show incomplete compensation, tolerating small but sustained residual errors that persist despite repeated trials. State-space models explain this residual asymptotic error as interplay between learning from error and reversion to baseline, a form of forgetting. Previous wor...
Movement variability is often considered an unwanted byproduct of a noisy nervous system. However, variability can signal a form of implicit exploration, indicating that the nervous system is intentionally varying the motor commands in search of actions that yield the greatest success. Here, we investigated the role of the human basal ganglia in co...
Autism spectrum disorder is a developmental disorder characterized by deficits in social and communication skills and repetitive and stereotyped interests and behaviours. Although not part of the diagnostic criteria, individuals with autism experience a host of motor impairments, potentially due to abnormalities in how they learn motor control thro...
In motor tasks, efficiency can be measured via the commands that are produced to accomplish a goal. To maximize efficiency, the nervous system should produce task-relevant motor commands, while avoiding behaviors that are task-irrelevant. The current view is that this is achieved through training, i.e., the optimum motor commands are learned by tri...
Learning to control our movements is accompanied by neuroplasticity of motor areas of the brain. The mechanisms of neuroplasticity are diverse and produce what is referred to as the motor engram, i.e., the neural trace of the motor memory. Transcranial direct current stimulation (tDCS) alters the neural and behavioral correlates of motor learning,...
The current view of motor learning suggests that when we revisit a task, the brain recalls the motor commands it previously
learned. In this view, motor memory is a memory of motor commands, acquired through trial-and-error and reinforcement. Here
we show that the brain controls how much it is willing to learn from the current error through a princ...
Background: Theory suggests that motor learning either underlies or parallels learning of social and communication skills, deficits of which are at the core of autism spectrum disorder (ASD). Children with ASD demonstrate both hyper- and hypo-sensitivity to sensory stimuli, as well as generalized motor impairments. Specifically, studies of motor le...
We investigated the contributions of the cerebellum and the motor cortex (M1) to acquisition and retention of human motor memories in a force field reaching task. We found that anodal transcranial direct current stimulation (tDCS) of the cerebellum, a technique that is thought to increase neuronal excitability, increased the ability to learn from e...
We have two arms, many muscles in each arm, and numerous neurons that contribute to their control. How does the brain assign responsibility to each of these potential actors? We considered a bimanual task in which people chose how much force to produce with each arm so that the sum would equal a target. We found that the dominant arm made a greater...
A study demonstrates that variability in how people perform a movement can predict the rate of motor learning on an individual basis. This suggests that motor 'noise' is a central component of motor learning.
If we assume that the purpose of a movement is to acquire a rewarding state, the duration of the movement carries a cost because it delays acquisition of reward. For some people, passage of time carries a greater cost, as evidenced by how long they are willing to wait for a rewarding outcome. These steep discounters are considered impulsive. Is the...
A recent neurophysiology study provides data from the cerebellar vermis/nodulus, where neurons encode translation of the head, even when these translations are induced via an illusion. These data provide new neurophysiological evidence that the cerebellum is important for computations involving internal models of motion, estimating the state of the...
When motor commands are accompanied by an unexpected outcome, the resulting error induces changes in subsequent commands. However, when errors are artificially eliminated, changes in motor commands are not sustained but show decay. Why does the adaptation-induced change in motor output decay in the absence of error? A prominent idea is that decay r...
Both abrupt and gradually imposed perturbations produce adaptive changes in motor output, but the neural basis of adaptation may be distinct. Here, we measured the state of the motor cortex (M1) and the corticospinal network during adaptation by measuring motor evoked potentials (MEPs) before reach onset using transcranial magnetic stimulation of M...
Suppose that the purpose of a movement is to place the body in a more rewarding state. In this framework, slower movements may increase accuracy and therefore improve the probability of acquiring reward, but the longer durations of slow movements produce devaluation of reward. Here we hypothesize that the brain decides the vigor of a movement (dura...
In a voluntary movement, the nervous system specifies not only the motor commands but also the gains associated with reaction to sensory feedback. For example, suppose that, during reaching, a perturbation tends to push the hand to the left. With practice, the brain not only learns to produce commands that predictively compensate for the perturbati...
It has been proposed that the brain predicts the sensory consequences of a movement and compares it to the actual sensory feedback. When the two differ, an error signal is formed, driving adaptation. How does an error in one trial alter performance in the subsequent trial? Here we show that the sensitivity to error is not constant but declines as a...
The brain builds an association between action and sensory feedback to predict the sensory consequence of self-generated motor commands. This internal model of action is central to our ability to adapt movements and may also play a role in our ability to learn from observing others. Recently, we reported that the spatial generalization patterns tha...
When we use a novel tool, the motor commands may not produce the expected outcome. In healthy individuals, with practice the brain learns to alter the motor commands. This change depends critically on the cerebellum as damage to this structure impairs adaptation. However, it is unclear precisely what the cerebellum contributes to the process of ada...
The kinematics of elementary movements such as saccadic eye movements are highly regular across repeated movements and across individuals. Historically, saccades have been viewed as following a fixed kinematic pattern with a characteristic peak velocity and duration that varies only with the amplitude of movement. Here we show experimentally in hum...
