State Estimation in the Cerebellum

An exciting hypothesis about the cerebellum is that its role is one of state estimation—a process that combines afferent copies of motor commands with afferent sensory signals to produce a representation of the current status of the peripheral motor system. Sensory inputs alone cannot provide a perfect state signal because of inevitable delays in their afferent pathways. We have recently reported the effects of transcranial magnetic stimulation (TMS) over the ipsilateral cerebellum as healthy subjects made rapid reaching movements towards visually defined targets (Miall et al. in PLoS Biology 5:2733–2744, 2007). Errors in the initial direction and in the final finger position of this reachto-target movement were consistent with the reaching movements being planned and initiated from an estimated hand position that was about 138 ms out of date. This interval is consistent with estimates of the delays in sensory motor pathways that would inform the central nervous system of the peripheral status. We now report new data using the same paradigm, testing the effects of varying the TMS stimulus train from one, two, or three pulses. We show that the errors in movement are relatively insensitive to the TMS pulse-train duration. The estimated time interval by which the hand position is mislocalized varied by only 12 ms as the TMS train duration increased by 100 ms. Thus, this interval is likely to reflect physiological processes within the cerebellum rather than the TMSstimulus duration. This new evidence supports our earlier claim that the cerebellum is responsible for predictively updating a central state estimate over an interval of about 120–140 ms. Dysfunction of the cerebellum, whether through disease or experimental procedures, leads to motor errors consistent with a loss of knowledge of the true state of the motor system

Remembering Forward: Neural Correlates of Memory and Prediction in Human Motor Adaptation

We used functional MR imaging (FMRI), a robotic manipulandum and systems identification techniques to examine neural correlates of predictive compensation for spring-like loads during goal-directed wrist movements in neurologically-intact humans. Although load changed unpredictably from one trial to the next, subjects nevertheless used sensorimotor memories from recent movements to predict and compensate upcoming loads. Prediction enabled subjects to adapt performance so that the task was accomplished with minimum effort. Population analyses of functional images revealed a distributed, bilateral network of cortical and subcortical activity supporting predictive load compensation during visual target capture. Cortical regions – including prefrontal, parietal and hippocampal cortices – exhibited trial-by-trial fluctuations in BOLD signal consistent with the storage and recall of sensorimotor memories or “states” important for spatial working memory. Bilateral activations in associative regions of the striatum demonstrated temporal correlation with the magnitude of kinematic performance error (a signal that could drive reward-optimizing reinforcement learning and the prospective scaling of previously learned motor programs). BOLD signal correlations with load prediction were observed in the cerebellar cortex and red nuclei (consistent with the idea that these structures generate adaptive fusimotor signals facilitating cancelation of expected proprioceptive feedback, as required for conditional feedback adjustments to ongoing motor commands and feedback error learning). Analysis of single subject images revealed that predictive activity was at least as likely to be observed in more than one of these neural systems as in just one. We conclude therefore that motor adaptation is mediated by predictive compensations supported by multiple, distributed, cortical and subcortical structures

Attentive Learning of Sequential Handwriting Movements: A Neural Network Model

Defense Advanced research Projects Agency and the Office of Naval Research (N00014-95-1-0409, N00014-92-J-1309); National Science Foundation (IRI-97-20333); National Institutes of Health (I-R29-DC02952-01)

Recurrent cerebellar architecture solves the motor-error problem

Current views of cerebellar function have been heavily influenced by the models of Marr and Albus, who suggested that the climbing fibre input to the cerebellum acts as a teaching signal for motor learning. It is commonly assumed that this teaching signal must be motor error (the difference between actual and correct motor command), but this approach requires complex neural structures to estimate unobservable motor error from its observed sensory consequences. We have proposed elsewhere a recurrent decorrelation control architecture in which Marr-Albus models learn without requiring motor error. Here, we prove convergence for this architecture and demonstrate important advantages for the modular control of systems with multiple degrees of freedom. These results are illustrated by modelling adaptive plant compensation for the three-dimensional vestibular ocular reflex. This provides a functional role for recurrent cerebellar connectivity, which may be a generic anatomical feature of projections between regions of cerebral and cerebellar cortex

Respiratory, postural and spatio-kinetic motor stabilization, internal models, top-down timed motor coordination and expanded cerebello-cerebral circuitry: a review

Human dexterity, bipedality, and song/speech vocalization in Homo are reviewed within a motor evolution perspective in regard to 

(i) brain expansion in cerebello-cerebral circuitry, 
(ii) enhanced predictive internal modeling of body kinematics, body kinetics and action organization, 
(iii) motor mastery due to prolonged practice, 
(iv) task-determined top-down, and accurately timed feedforward motor adjustment of multiple-body/artifact elements, and 
(v) reduction in automatic preflex/spinal reflex mechanisms that would otherwise restrict such top-down processes. 

Dual-task interference and developmental neuroimaging research argues that such internal modeling based motor capabilities are concomitant with the evolution of 
(vi) enhanced attentional, executive function and other high-level cognitive processes, and that 
(vii) these provide dexterity, bipedality and vocalization with effector nonspecific neural resources. 

The possibility is also raised that such neural resources could 
(viii) underlie human internal model based nonmotor cognitions. 
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A Scalable Model of Cerebellar Adaptive Timing and Sequencing: The Recurrent Slide and Latch (RSL) Model

From the dawn of modern neural network theory, the mammalian cerebellum has been a favored object of mathematical modeling studies. Early studies focused on the fan-out, convergence, thresholding, and learned weighting of perceptual-motor signals within the cerebellar cortex. This led in the proposals of Albus (1971; 1975) and Marr (1969) to the still viable idea that the granule cell stage in the cerebellar cortex performs a sparse expansive recoding of the time-varying input vector. This recoding reveals and emphasizes combinations (of input state variables) in a distributed representation that serves as a basis for the learned, state-dependent control actions engendered by cerebellar outputs to movement related centers. Although well-grounded as such, this perspective seriously underestimates the intelligence of the cerebellar cortex. Context and state information arises asynchronously due to the heterogeneity of sources that contribute signals to compose the cerebellar input vector. These sources include radically different sensory systems - vision, kinesthesia, touch, balance and audition - as well as many stages of the motor output channel. To make optimal use of available signals, the cerebellum must be able to sift the evolving state representation for the most reliable predictors of the need for control actions, and to use those predictors even if they appear only transiently and well in advance of the optimal time for initiating the control action. Such a cerebellar adaptive timing competence has recently been experimentally verified (Perrett, Ruiz, & Mauk, 1993). This paper proposes a modification to prior, population, models for cerebellar adaptive timing and sequencing. Since it replaces a population with a single clement, the proposed Recurrent Slide and Latch (RSL) model is in one sense maximally efficient, and therefore optimal from the perspective of scalability.Defense Advanced Research Projects Agency and the Office of Naval Research (N00014-92-J-1309, N00014-93-1-1364, N00014-95-1-0409)

Cortical Models for Movement Control

Defense Advanced Research Projects Agency and Office of Naval Research (N0014-95-l-0409)

The cerebellum could solve the motor error problem through error increase prediction

We present a cerebellar architecture with two main characteristics. The first one is that complex spikes respond to increases in sensory errors. The second one is that cerebellar modules associate particular contexts where errors have increased in the past with corrective commands that stop the increase in error. We analyze our architecture formally and computationally for the case of reaching in a 3D environment. In the case of motor control, we show that there are synergies of this architecture with the Equilibrium-Point hypothesis, leading to novel ways to solve the motor error problem. In particular, the presence of desired equilibrium lengths for muscles provides a way to know when the error is increasing, and which corrections to apply. In the context of Threshold Control Theory and Perceptual Control Theory we show how to extend our model so it implements anticipative corrections in cascade control systems that span from muscle contractions to cognitive operations.Comment: 34 pages (without bibliography), 13 figure