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Corticostriatal dynamics encode the refinement of specific behavioral variability during skill learning.

Santos FJ, Oliveira RF, Jin X, Costa RM - Elife (2015)

Bottom Line: Animals trained to perform progressively faster sequences of lever presses to obtain reinforcement reduced variability in sequence frequency, but increased variability in an orthogonal feature (sequence duration).Corticostriatal plasticity was required for the reduction in frequency variability, but not for variability in sequence duration.These data suggest that during motor learning corticostriatal dynamics encode the refinement of specific behavioral features that change the probability of obtaining outcomes.

View Article: PubMed Central - PubMed

Affiliation: Champalimaud Neuroscience Programme, Fundação Champalimaud, Lisbon, Portugal.

ABSTRACT
Learning to perform a complex motor task requires the optimization of specific behavioral features to cope with task constraints. We show that when mice learn a novel motor paradigm they differentially refine specific behavioral features. Animals trained to perform progressively faster sequences of lever presses to obtain reinforcement reduced variability in sequence frequency, but increased variability in an orthogonal feature (sequence duration). Trial-to-trial variability of the activity of motor cortex and striatal projection neurons was higher early in training and subsequently decreased with learning, without changes in average firing rate. As training progressed, variability in corticostriatal activity became progressively more correlated with behavioral variability, but specifically with variability in frequency. Corticostriatal plasticity was required for the reduction in frequency variability, but not for variability in sequence duration. These data suggest that during motor learning corticostriatal dynamics encode the refinement of specific behavioral features that change the probability of obtaining outcomes.

No MeSH data available.


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Behavior variability is differentially modulated during training.(A, B) Comparison of frequency and duration between reinforced (RF) and non-reinforced (Non-RF) sequences. (C, D) Variance and (E, F) variability, measured as the Fano factor, for reinforced and non-reinforced sequences. Black lines correspond to mean values for non-reinforced sequences. Red lines correspond to mean values for reinforced sequences. Shaded areas correspond to mean ± SEM.DOI:http://dx.doi.org/10.7554/eLife.09423.008
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fig3: Behavior variability is differentially modulated during training.(A, B) Comparison of frequency and duration between reinforced (RF) and non-reinforced (Non-RF) sequences. (C, D) Variance and (E, F) variability, measured as the Fano factor, for reinforced and non-reinforced sequences. Black lines correspond to mean values for non-reinforced sequences. Red lines correspond to mean values for reinforced sequences. Shaded areas correspond to mean ± SEM.DOI:http://dx.doi.org/10.7554/eLife.09423.008

Mentions: To further investigate this, we analyzed if the variability of these two behavioral dimensions was different in reinforced vs non-reinforced sequences (Figure 3). We verified that sequences leading to reinforcement had indeed significantly lower variability in frequency compared to non-reinforced sequences (main effect of reinforcement, F1,38 = 7.608, p = 0.0089, Figure 3C and F1,38 = 28.34, p < 0.0001, Figure 3E), but there were no significant differences in the variability of sequence duration between reinforced and non-reinforced sequences (Figure 3D,F). These results suggest that mice selectively reduced variability in the behavioral domains where variability affected the probability of reinforcement (sequence frequency), but not in domains where variability did not change this probability (sequence duration).10.7554/eLife.09423.008Figure 3.Behavior variability is differentially modulated during training.


Corticostriatal dynamics encode the refinement of specific behavioral variability during skill learning.

Santos FJ, Oliveira RF, Jin X, Costa RM - Elife (2015)

Behavior variability is differentially modulated during training.(A, B) Comparison of frequency and duration between reinforced (RF) and non-reinforced (Non-RF) sequences. (C, D) Variance and (E, F) variability, measured as the Fano factor, for reinforced and non-reinforced sequences. Black lines correspond to mean values for non-reinforced sequences. Red lines correspond to mean values for reinforced sequences. Shaded areas correspond to mean ± SEM.DOI:http://dx.doi.org/10.7554/eLife.09423.008
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getmorefigures.php?uid=PMC4616249&req=5

fig3: Behavior variability is differentially modulated during training.(A, B) Comparison of frequency and duration between reinforced (RF) and non-reinforced (Non-RF) sequences. (C, D) Variance and (E, F) variability, measured as the Fano factor, for reinforced and non-reinforced sequences. Black lines correspond to mean values for non-reinforced sequences. Red lines correspond to mean values for reinforced sequences. Shaded areas correspond to mean ± SEM.DOI:http://dx.doi.org/10.7554/eLife.09423.008
Mentions: To further investigate this, we analyzed if the variability of these two behavioral dimensions was different in reinforced vs non-reinforced sequences (Figure 3). We verified that sequences leading to reinforcement had indeed significantly lower variability in frequency compared to non-reinforced sequences (main effect of reinforcement, F1,38 = 7.608, p = 0.0089, Figure 3C and F1,38 = 28.34, p < 0.0001, Figure 3E), but there were no significant differences in the variability of sequence duration between reinforced and non-reinforced sequences (Figure 3D,F). These results suggest that mice selectively reduced variability in the behavioral domains where variability affected the probability of reinforcement (sequence frequency), but not in domains where variability did not change this probability (sequence duration).10.7554/eLife.09423.008Figure 3.Behavior variability is differentially modulated during training.

Bottom Line: Animals trained to perform progressively faster sequences of lever presses to obtain reinforcement reduced variability in sequence frequency, but increased variability in an orthogonal feature (sequence duration).Corticostriatal plasticity was required for the reduction in frequency variability, but not for variability in sequence duration.These data suggest that during motor learning corticostriatal dynamics encode the refinement of specific behavioral features that change the probability of obtaining outcomes.

View Article: PubMed Central - PubMed

Affiliation: Champalimaud Neuroscience Programme, Fundação Champalimaud, Lisbon, Portugal.

ABSTRACT
Learning to perform a complex motor task requires the optimization of specific behavioral features to cope with task constraints. We show that when mice learn a novel motor paradigm they differentially refine specific behavioral features. Animals trained to perform progressively faster sequences of lever presses to obtain reinforcement reduced variability in sequence frequency, but increased variability in an orthogonal feature (sequence duration). Trial-to-trial variability of the activity of motor cortex and striatal projection neurons was higher early in training and subsequently decreased with learning, without changes in average firing rate. As training progressed, variability in corticostriatal activity became progressively more correlated with behavioral variability, but specifically with variability in frequency. Corticostriatal plasticity was required for the reduction in frequency variability, but not for variability in sequence duration. These data suggest that during motor learning corticostriatal dynamics encode the refinement of specific behavioral features that change the probability of obtaining outcomes.

No MeSH data available.


Related in: MedlinePlus