Gating of neural error signals during motor learning

Abstract

Cerebellar climbing fiber activity encodes performance errors during many motor learning tasks, but the role of these error signals in learning has been controversial. We compared two motor learning paradigms that elicited equally robust putative error signals in the same climbing fibers: learned increases and decreases in the gain of the vestibulo-ocular reflex (VOR). During VOR-increase training, climbing fiber activity on one trial predicted changes in cerebellar output on the next trial, and optogenetic activation of climbing fibers to mimic their encoding of performance errors was sufficient to implant a motor memory. In contrast, during VOR-decrease training, there was no trial-by-trial correlation between climbing fiber activity and changes in cerebellar output, and climbing fiber activation did not induce VOR-decrease learning. Our data suggest that the ability of climbing fibers to induce plasticity can be dynamically gated in vivo, even under conditions where climbing fibers are robustly activated by performance errors.DOI: http://dx.doi.org/10.7554/eLife.02076.001

Timing Rules for Synaptic Plasticity Matched to Behavioral Function

“…It was recently reported that a single spike in a climbing fiber in vivo can induce plasticity (Kimpo et al, 2014;Medina and Lisberger, 2008;Yang and Lisberger, 2010). We tested whether there was short-term plasticity at the PF-to-PC synapses in response to a single pairing of parallel fiber and climbing fiber activation (see also Brenowitz and Regehr, 2005), which could support the single-trial plasticity observed in vivo during motor learning.…”

“…Long-term associative plasticity in the flocculus in vitro: Temporal requirements matched to behavioral function Our finding that coincident parallel fiber and climbing fiber stimulation failed to induce LTD in the flocculus was surprising, given the multiple lines of evidence for a role of climbing fiber-triggered LTD in flocculus-dependent learning (e.g., Boyden et al, 2006;Hansel et al, 2006;Ito, 2001;Kimpo et al, 2014;Medina and Lisberger, 2008). However, in vivo, the activation of climbing fibers by performance errors would be delayed relative to the parallel fiber activity that caused the error, rather than coincident.…”

“…During oculomotor learning, a spike in a climbing fiber on one trial is associated with a suppression of firing in its Purkinje cell target on the next trial (Kimpo et al, 2014;Medina and Lisberger, 2008;Lisberger, 2010, 2014). The temporal precision of this single-trial plasticity reported in vivo had appeared to be significantly less than what we found at the PF-to-PC synapses in vitro (hundreds of milliseconds vs. tens of milliseconds).…”

“…2B) suggested that plasticity might occur at synapses active in a specific time window preceding the climbing fiber spike. Therefore, we aligned changes in Purkinje cell firing during VOR learning in rhesus monkeys (Kimpo et al, 2014) to the time of the climbing fiber spike in the preceding trial (Fig. 2C, Fig.…”

Cerebellar Encoding of Multiple Candidate Error Cues in the Service of Motor Learning

“…The VOR presumably evolved to stabilize large-field, rather than foveal, images, because it is a phylogenetically primitive oculomotor behavior that functions in species without a fovea. Accordingly, VOR learning can be induced by pairing passive head motion with coherent, large-field image motion (Ito et al, 1974;Miles and Fuller, 1974;Gonshor and Jones, 1976;Robinson, 1976;Watanabe, 1984). In primates, however, the oculomotor system has evolved the ability to track a small object of interest, using smooth pursuit eye movements.…”