Coordinated cerebellar climbing fiber activity signals learned sensorimotor predictions

AbstractThe prevailing model of cerebellar learning states that climbing fibers (CFs) are both driven by, and serve to correct, erroneous motor output. However, this model is grounded largely in studies of behaviors that utilize hardwired neural pathways to link sensory input to motor output. To test whether this model applies to more flexible learning regimes that require arbitrary sensorimotor associations, we have developed a cerebellar-dependent motor learning paradigm compatible with both mesoscale and single dendrite resolution calcium imaging in mice. Here, we find that CFs are preferentially driven by and more time-locked to correctly executed movements and other task parameters that predict reward outcome, exhibiting widespread correlated activity within parasagittal processing zones that is governed by these predictions. Together, such CF activity patterns are well-suited to drive learning by providing predictive instructional input consistent with an unsigned reinforcement learning signal that does not rely exclusively on motor errors.

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Retention of Hindlimb Stepping Ability in Adult Spinal Cats After the Cessation of Step Training

Journal of Neurophysiology ◽

10.1152/jn.1999.81.1.85 ◽

1999 ◽

Vol 81 (1) ◽

pp. 85-94 ◽

Cited By ~ 105

Author(s):

R. D. De Leon ◽

J. A. Hodgson ◽

R. R. Roy ◽

V. R. Edgerton

Keyword(s):

Weight Bearing ◽

Activity Patterns ◽

Motor Task ◽

Full Weight Bearing ◽

Electromyographic Activity ◽

Locomotor Training ◽

Neural Pathways ◽

Step Cycle ◽

Rapid Learning ◽

Hindlimb Muscle

de Leon, R. D., J. A. Hodgson, R. R. Roy, and V. R. Edgerton. Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J. Neurophysiol. 81: 85–94, 1999. Adult spinal cats were trained to perform bipedal hindlimb locomotion on a treadmill for 6–12 wk. After each animal acquired the ability to step, locomotor training was withheld, and stepping was reexamined 6 and 12 wk after training ended. The performance characteristics, hindlimb muscle electromyographic activity patterns, and kinematic characteristics of the step cycle that were acquired with training were largely maintained when training was withheld for 6 wk. However, after 12 wk without training, locomotor performance declined, i.e., stumbling was more frequent, and the ability to consistently execute full weight-bearing steps at any treadmill speed decreased. In addition, the height that the paw was lifted during the swing phase decreased, and a smaller range of extension in the hindlimbs occurred during the E3 phase of stance. When three of the spinal cats underwent 1 wk of retraining, stepping ability was regained more rapidly than when trained initially. The finding that stepping ability in trained adult spinal cats can persist for 6 wk without training provides further evidence that training-induced enhancement of stepping is learned in the spinal cats and that a memory of the enhanced stepping is stored in the spinal networks. However, it appears that the spinal cord can forget how to consistently execute stepping if that task is not practiced for 12 wk. The more rapid learning that occurred with retraining is also consistent with a learning phenomenon. These results in conjunction with our earlier findings suggest that the efficacy of the neural pathways that execute a motor task is highly dependent on the periodic activation of those pathways in a sequence compatible with that motor task.

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Macphail (1987) Revisited: Pigeons Have Much Cognitive Behavior in Common With Humans

Frontiers in Psychology ◽

10.3389/fpsyg.2020.618636 ◽

2021 ◽

Vol 11 ◽

Author(s):

Thomas R. Zentall

Keyword(s):

Cognitive Ability ◽

Present Article ◽

Sensory Input ◽

Motor Output ◽

Cognitive Behavior ◽

Intellectual Abilities ◽

Intelligent Behavior

The hypothesis proposed by Macphail (1987) is that differences in intelligent behavior thought to distinguish different species were likely attributed to differences in the context of the tasks being used. Once one corrects for differences in sensory input, motor output, and incentive, it is likely that all vertebrate animals have comparable intellectual abilities. In the present article I suggest a number of tests of this hypothesis with pigeons. In each case, the evidence suggests that either there is evidence for the cognitive behavior, or the pigeons suffer from biases similar to those of humans. Thus, Macphail’s hypothesis offers a challenge to researchers to find the appropriate conditions to bring out in the animal the cognitive ability being tested.

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Neuronal Activity in the Rodent Dorsal Striatum in Sequential Navigation: Separation of Spatial and Reward Responses on the Multiple T Task

Journal of Neurophysiology ◽

10.1152/jn.00687.2003 ◽

2004 ◽

Vol 91 (5) ◽

pp. 2259-2272 ◽

Cited By ~ 97

Author(s):

Neil Schmitzer-Torbert ◽

A. David Redish

Keyword(s):

Reinforcement Learning ◽

Spatial Representation ◽

Sensory Input ◽

Learning Algorithm ◽

Dorsal Striatum ◽

Food Delivery ◽

Simple Motor ◽

Experimental Approaches ◽

Highly Correlated ◽

To Receive

The striatum plays an important role in “habitual” learning and memory and has been hypothesized to implement a reinforcement-learning algorithm to select actions to perform given the current sensory input. Many experimental approaches to striatal activity have made use of temporally structured tasks, which imply that the striatal representation is temporal. To test this assumption, we recorded neurons in the dorsal striatum of rats running a sequential navigation task: the multiple T maze. Rats navigated a sequence of four T maze turns to receive food rewards delivered in two locations. The responses of neurons that fired phasically were examined. Task-responsive phasic neurons were active as rats ran on the maze (maze-responsive) or during reward receipt (reward-responsive). Neither mazenor reward-responsive neurons encoded simple motor commands: maze-responses were not well correlated with the shape of the rat's path and most reward-responsive neurons did not fire at similar rates at both food-delivery sites. Maze-responsive neurons were active at one or more locations on the maze, but these responses did not cluster at spatial landmarks such as turns. Across sessions the activity of maze-responsive neurons was highly correlated when rats ran the same maze. Maze-responses encoded the location of the rat on the maze and imply a spatial representation in the striatum in a task with prominent spatial demands. Maze-responsive and reward-responsive neurons were two separate populations, suggesting a divergence in striatal information processing of navigation and reward.

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Internal Representations of Sensory Input Reflect the Motor Output with Which Organisms Respond to the Input

Seeing, Thinking and Knowing ◽

10.1007/1-4020-2081-3_6 ◽

2004 ◽

pp. 115-141 ◽

Cited By ~ 8

Author(s):

Andrea Di Ferdinando ◽

Domenico Parisi

Keyword(s):

Sensory Input ◽

Motor Output ◽

Internal Representations

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Expecting to Teach Enhances Learning: Evidence From a Motor Learning Paradigm

Journal of Motor Learning and Development ◽

10.1123/jmld.2015-0036 ◽

2016 ◽

Vol 4 (2) ◽

pp. 197-207 ◽

Cited By ~ 8

Author(s):

Marcos Daou ◽

Taylor L. Buchanan ◽

Kyle R. Lindsey ◽

Keith R. Lohse ◽

Matthew W. Miller

Keyword(s):

Motor Learning ◽

Learning Paradigm

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Spontaneous activations follow a common developmental course across primary sensory areas in mouse neocortex

Journal of Neurophysiology ◽

10.1152/jn.00172.2016 ◽

2016 ◽

Vol 116 (2) ◽

pp. 431-437 ◽

Cited By ~ 6

Author(s):

Charles G. Frye ◽

Jason N. MacLean

Keyword(s):

Calcium Imaging ◽

Sensory Input ◽

Primary Auditory Cortex ◽

Developmental Trajectory ◽

Two Photon ◽

Developmental Progression ◽

Sensory Modalities ◽

Spatially Distributed ◽

And Function ◽

Insight Into

Spontaneous propagation of spiking within the local neocortical circuits of mature primary sensory areas is highly nonrandom, engaging specific sets of interconnected and functionally related neurons. These spontaneous activations promise insight into neocortical structure and function, but their properties in the first 2 wk of perinatal development are incompletely characterized. Previously, we have found that there is a minimal numerical sample, on the order of 400 cells, necessary to fully capture mature neocortical circuit dynamics. Therefore we maximized our numerical sample by using two-photon calcium imaging to observe spontaneous activity in populations of up to 1,062 neurons spanning multiple columns and layers in 52 acute coronal slices of mouse neocortex at each day from postnatal day (PND) 3 to PND 15. Slices contained either primary auditory cortex (A1) or somatosensory barrel field (S1BF), which allowed us to compare sensory modalities with markedly different developmental timelines. Between PND 3 and PND 8, populations in both areas exhibited activations of anatomically compact subgroups on the order of dozens of cells. Between PND 9 and PND 13, the spatiotemporal structure of the activity diversified to include spatially distributed activations encompassing hundreds of cells. Sparse activations covering the entire field of view dominated in slices taken on or after PND 14. These and other findings demonstrate that the developmental progression of spontaneous activations from active local modules in the first postnatal week to sparse, intermingled groups of neurons at the beginning of the third postnatal week generalizes across primary sensory areas, consistent with an intrinsic developmental trajectory independent of sensory input.

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Phase-Amplitude Markers of Synchrony and Noise: A Resting-State and TMS-EEG Study of Schizophrenia

Cerebral Cortex Communications ◽

10.1093/texcom/tgaa013 ◽

2020 ◽

Vol 1 (1) ◽

Author(s):

Dominik Freche ◽

Jodie Naim-Feil ◽

Shmuel Hess ◽

Avraham Peled ◽

Alexander Grinshpoon ◽

...

Keyword(s):

Resting State ◽

Narrow Band ◽

Signal To Noise Ratio ◽

Phase Locking ◽

Activity Patterns ◽

Neuronal Populations ◽

Correlated Activity ◽

Amplitude Fluctuations ◽

Phase Amplitude ◽

External Stimuli

Abstract The electroencephalogram (EEG) of schizophrenia patients is known to exhibit a reduction of signal-to-noise ratio and of phase locking, as well as a facilitation of excitability, in response to a variety of external stimuli. Here, we demonstrate these effects in transcranial magnetic stimulation (TMS)-evoked potentials and in the resting-state EEG. To ensure veracity, we used 3 weekly sessions and analyzed both resting-state and TMS-EEG data. For the TMS responses, our analysis verifies known results. For the resting state, we introduce the methodology of mean-normalized variation to the EEG analysis (quartile-based coefficient of variation), which allows for a comparison of narrow-band EEG amplitude fluctuations to narrow-band Gaussian noise. This reveals that amplitude fluctuations in the delta, alpha, and beta bands of healthy controls are different from those in schizophrenia patients, on time scales of tens of seconds. We conclude that the EEG-measured cortical activity patterns of schizophrenia patients are more similar to noise, both in alpha- and beta-resting state and in TMS responses. Our results suggest that the ability of neuronal populations to form stable, locally, and temporally correlated activity is reduced in schizophrenia, a conclusion, that is, in accord with previous experiments on TMS-EEG and on resting-state EEG.

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Self-organization of cortical areas in the development and evolution of neocortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2011724117 ◽

2020 ◽

Vol 117 (46) ◽

pp. 29212-29220 ◽

Cited By ~ 1

Author(s):

Nabil Imam ◽

Barbara L. Finlay

Keyword(s):

Activity Patterns ◽

Basic Mechanism ◽

Physical Parameters ◽

Network Growth ◽

Cortical Areas ◽

Mirror Reversal ◽

Correlated Activity ◽

The Matrix ◽

Characteristic Features ◽

Development And Evolution

While the mechanisms generating the topographic organization of primary sensory areas in the neocortex are well studied, what generates secondary cortical areas is virtually unknown. Using physical parameters representing primary and secondary visual areas as they vary from monkey to mouse, we derived a network growth model to explore if characteristic features of secondary areas could be produced from correlated activity patterns arising from V1 alone. We found that V1 seeded variable numbers of secondary areas based on activity-driven wiring and wiring-density limits within the cortical surface. These secondary areas exhibited the typical mirror-reversal of map topography on cortical area boundaries and progressive reduction of the area and spatial resolution of each new map on the caudorostral axis. Activity-based map formation may be the basic mechanism that establishes the matrix of topographically organized cortical areas available for later computational specialization.

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