Neural mechanisms underlying the reduction in behavioral variability during trial-and-error learning
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1
Ecole Normale Superieure Cachan , France
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2
Harvard University, OEB and CBS, United States
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3
Harvard University, Center for Brain Science, United States
Motor exploration is essential for trial-and-error learning, yet as learning progresses motor variability is often reduced to yield a stereotyped performance. Here we explore the neural mechanisms underlying this reduction in behavioral variability and how it relates to the learning-driven maturation of motor circuits in the zebra finch, a songbird that shows decreased vocal variability with song learning. Song variability is driven by a basal ganglia circuit that projects to the motor cortex analogue brain region RA through nucleus LMAN [1]. In very young songbirds variable LMAN activity dominates the motor program [2], resulting in variable vocalizations, but as learning progresses, HVC, a premotor area providing the other main input to RA, takes over and, in adult birds, drives a precise and robust song through its stereotyped input to RA. The song learning process is thought to be driven by synaptic reorganization in the HVC-RA network, yet the variable LMAN input to RA remains intact also in adult birds: If HVC is lesioned, LMAN is capable of driving highly variable song, similar to what is observed in young birds [2] [3]. In this study, we examine the extent to which LMAN induced variability is reduced as a consequence of the strengthening and pruning of HVC-RA synapses. In our model of the HVC-RA-LMAN circuit, RA neurons are driven by temporally precise inputs from HVC and by random Poisson spike trains from LMAN. Maturation of HVC-RA synapses is modeled as a gradual shift from broadly distributed synaptic strengths to a more bimodal distribution, while synaptic inputs from LMAN to RA are kept fixed. Comparing our model with recordings from RA projection neurons made in juvenile zebra finches during singing, we can account for two distinct trends observed in the recordings: (1) Firing patterns gradually become more sparse and bursty, with stereotyped, higher firing rate events emerging. (2) Trial-to-trial variability of RA firing patterns is gradually reduced with age. Furthermore, our model predicts that at any given age LMAN’s effect on variability in RA should depend on the instantaneous firing rate of RA bursts. Analysis of song-aligned spike trains from RA neurons recorded in zebra finches of different ages confirmed this prediction, showing a strong statistical relationship between firing rate and variability. In agreement with the model, this relationship depends only weakly on age, whereas the distribution of firing rates significantly evolves as learning progresses. Our results suggest a direct mechanistic link between the shaping and maturation of a learned motor program and the reduction in behavioral variability.
References
1. Olveczky BP, Andalman AS, Fee MS (2005) Vocal Experimentation in the Juvenile Songbird Requires a Basal Ganglia Circuit. PLoS Biol 3(5): e153.
2. Aronov D, Andalman AS, Fee MS . 2008. A specialized forebrain circuit for vocal babbling in the juvenile songbird Science 320 630-634.
3. Thompson, J.A., Wu, W., Bertram, R. & Johnson, F. Auditory-dependent vocal recovery in adult male zebra finches is facilitated by lesion of a forebrain pathway that includes the basal ganglia. J. Neurosci. 27, 12308-12320 (2007).
Conference:
Computational and Systems Neuroscience 2010, Salt Lake City, UT, United States, 25 Feb - 2 Mar, 2010.
Presentation Type:
Poster Presentation
Topic:
Poster session I
Citation:
Dubreuil
A,
Burak
Y,
Otchy
T and
Olveczky
B
(2010). Neural mechanisms underlying the reduction in behavioral variability during trial-and-error learning.
Front. Neurosci.
Conference Abstract:
Computational and Systems Neuroscience 2010.
doi: 10.3389/conf.fnins.2010.03.00097
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Received:
20 Feb 2010;
Published Online:
20 Feb 2010.
*
Correspondence:
Alexis Dubreuil, Ecole Normale Superieure Cachan, Paris, France, alexis.dubreuil@ens-cachan.fr