Changes in Purkinje Cell Simple Spike Encoding of Reach Kinematics during Adaption to a Mechanical Perturbation

Hewitt, Angela; Popa, Laurentiu S.; Ebner, Timothy J.

doi:10.1523/jneurosci.2579-14.2015

Cited by 40 publications

(49 citation statements)

References 76 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Such experiments find that the discharge of SSs sometimes increases rather than decreases after a CS [78][79][80]. These observations are interpreted as evidence that the activity of CSs and SSs is functionally independent and that the mossy fiber→granule cell→parallel fiber→Purkinje cell projection accounts for the modulation of SSs.…”

Section: Alternative Views Of Cerebellar Circuitrymentioning

confidence: 85%

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Barmack

Yakhnitsa

2015

Cerebellum

View full text Add to dashboard Cite

Climbing and mossy fibers comprise two distinct afferent paths to the cerebellum. Climbing fibers directly evoke a large multispiked action potential in Purkinje cells termed a "complex spike" (CS). By logical exclusion, the other class of Purkinje cell action potential, termed "simple spike" (SS), has often been attributed to activity conveyed by mossy fibers and relayed to Purkinje cells through granule cells. Here, we investigate the relative importance of climbing and mossy fiber pathways in modulating neuronal activity by recording extracellularly from Purkinje cells, as well as from mossy fiber terminals and interneurons in folia 8-10. Sinusoidal roll-tilt vestibular stimulation vigorously modulates the discharge of climbing and mossy fiber afferents, Purkinje cells, and interneurons in folia 9-10 in anesthetized mice. Roll-tilt onto the side ipsilateral to the recording site increases the discharge of both climbing fibers (CSs) and mossy fibers. However, the discharges of SSs decrease during ipsilateral roll-tilt. Unilateral microlesions of the beta nucleus (β-nucleus) of the inferior olive blocks vestibular modulation of both CSs and SSs in contralateral Purkinje cells. The blockage of SSs occurs even though primary and secondary vestibular mossy fibers remain intact. When mossy fiber afferents are damaged by a unilateral labyrinthectomy (UL), vestibular modulation of SSs in Purkinje cells ipsilateral to the UL remains intact. Two inhibitory interneurons, Golgi and stellate cells, could potentially contribute to climbing fiber-induced modulation of SSs. However, during sinusoidal roll-tilt, only stellate cells discharge appropriately out of phase with the discharge of SSs. Golgi cells discharge in phase with SSs. When the vestibularly modulated discharge is blocked by a microlesion of the inferior olive, the modulated discharge of CSs and SSs is also blocked. When the vestibular mossy fiber pathway is destroyed, vestibular modulation of ipsilateral CSs and SSs persists. We conclude that climbing fibers are primarily responsible for the vestibularly modulated discharge of both CSs and SSs. Modulation of the discharge of SSs is likely caused by climbing fiber-evoked stellate cell inhibition.

show abstract

Section: Alternative Views Of Cerebellar Circuitrymentioning

confidence: 85%

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Barmack

Yakhnitsa

2015

Cerebellum

View full text Add to dashboard Cite

show abstract

“…However, numerous other studies found no clear relationship between motor errors and CS activity or the discharge of neurons in the inferior olive, the origin of the climbing fiber projection, either during eye or limb movements (see [45]). A very recent study of adaptation of reaching movements to a mechanical perturbation demonstrated that the perturbation evoked a CS response in a very small percentage of Purkinje cells while the simple spike (SS) firing adapted in a majority of the neurons [46]. Also, new findings show that climbing fiber activation occurs and is correlated with changes in SS firing during increases in vestibulo-ocular reflex (VOR) gain but climbing fiber activation does not play a role in modifying SS firing during decreases in VOR gain [47, 48].…”

Section: Do Purkinje Cell Simple Spikes Encode Motor Errors Better Thmentioning

confidence: 99%

The Roles of the Olivocerebellar Pathway in Motor Learning and Motor Control. A Consensus Paper

et al. 2016

View full text Add to dashboard Cite

For many decades the predominant view in the cerebellar field has been that the olivocerebellar system's primary function is to induce plasticity in the cerebellar cortex, specifically, at the parallel fiber-Purkinje cell synapse. However, it has also long been proposed that the olivocerebellar system participates directly in motor control by helping to shape ongoing motor commands being issued by the cerebellum. Evidence consistent with both hypotheses exists; however, they are often investigated as mutually exclusive alternatives. In contrast, here we take the perspective that the olivocerebellar system can contribute to both the motor learning and motor control functions of the cerebellum, and might also play a role in development. We then consider the potential problems and benefits of its having multiple functions. Moreover, we discuss how its distinctive characteristics (e.g., low firing rates, synchronization, variable complex spike waveform) make it more or less suitable for one or the other of these functions, and why its having a dual role makes sense from an evolutionary perspective. We did not attempt to reach a consensus on the specific role(s) the olivocerebellar system plays in different types of movements, as that will ultimately be determined experimentally; however, collectively, the various contributions highlight the flexibility of the olivocerebellar system, and thereby suggest it has the potential to act in both the motor learning and motor control functions of the cerebellum.

show abstract

“…In the oculomotor vermis, increases in smooth pursuit gain involve increases in velocity coding in the summed Purkinje cell simple spike activity [50, 127]. Therefore, we recently investigated how the representation of kinematics in the simple spike discharge changes during reach adaptation [128]. …”

Section: Simple Spike and Complex Spike Changes During Reach Adaptationmentioning

confidence: 99%

“…The overall weak effect of the perturbation on the complex spike firing can also be appreciated from the population averages. All data are from Hewitt et al [128], with permission…”

Section: Figmentioning

confidence: 99%

The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning

et al. 2015

View full text Add to dashboard Cite

The cerebellum is essential for error-driven motor learning and is strongly implicated in detecting and correcting for motor errors. Therefore, elucidating how motor errors are represented in the cerebellum is essential in understanding cerebellar function, in general, and its role in motor learning, in particular. This review examines how motor errors are encoded in the cerebellar cortex in the context of a forward internal model that generates predictions about the upcoming movement and drives learning and adaptation. In this framework, sensory prediction errors, defined as the discrepancy between the predicted consequences of motor commands and the sensory feedback, are crucial for both on-line movement control and motor learning. While many studies support the dominant view that motor errors are encoded in the complex spike discharge of Purkinje cells, others have failed to relate complex spike activity with errors. Given these limitations, we review recent findings in the monkey showing that complex spike modulation is not necessarily required for motor learning or for simple spike adaptation. Also, new results demonstrate that the simple spike discharge provides continuous error signals that both lead and lag the actual movements in time, suggesting errors are encoded as both an internal prediction of motor commands and the actual sensory feedback. These dual error representations have opposing effects on simple spike discharge, consistent with the signals needed to generate sensory prediction errors used to update a forward internal model.

show abstract

Changes in Purkinje Cell Simple Spike Encoding of Reach Kinematics during Adaption to a Mechanical Perturbation

Cited by 40 publications

References 76 publications

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

The Roles of the Olivocerebellar Pathway in Motor Learning and Motor Control. A Consensus Paper

The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning

Contact Info

Product

Resources

About