Abstract
Excitatory and inhibitory synapses are the brain's most abundant synapse types. However, little is known about their formation during critical periods of motor skill learning, when sensory experience defines a motor target that animals strive to imitate. In songbirds, we find that exposure to tutor song leads to elimination of excitatory synapses in HVC (used here as a proper name), a key song generating brain area. A similar pruning is associated with song maturation, because juvenile birds have fewer excitatory synapses, the better their song imitations. In contrast, tutoring is associated with rapid insertion of inhibitory synapses, but the tutoring-induced structural imbalance between excitation and inhibition is eliminated during subsequent song maturation. Our work suggests that sensory exposure triggers the developmental onset of goal-specific motor circuits by increasing the relative strength of inhibition and it suggests a synapse-elimination model of song memorization.
Highlights
During critical period learning early in life, brain structure is regulated by intrinsic factors such as age, and by extrinsic factors including sensory experience (Andersen, 2003; Hubel and Wiesel, 1970; Kirkwood et al, 1995)
Using electron microscopy (EM), we investigated the effects of tutor song exposure on HVC synapses
We found that one day of tutor exposure led to a 26 ± 5% decrease in the HVC asymmetric synapse density (p = 3*10À9, linear mixed effect (LME) model with bird group as fixed effect and bird identity as random effect, df = 1152, n = 4 Short-tutored group (SHORT) birds and n = 4 isolated group (ISO) birds, see Materials and methods), Figure 1B,C
Summary
During critical period learning early in life, brain structure is regulated by intrinsic factors such as age, and by extrinsic factors including sensory experience (Andersen, 2003; Hubel and Wiesel, 1970; Kirkwood et al, 1995). During this period, neuronal connections are highly susceptible to experience-dependent modifications (Hensch, 2004), often manifest as competitive synapse elimination (Lichtman and Colman, 2000). Similar to human speech development (Neville and Bavelier, 2002), the normal development of birdsong requires early sensory experience (Barrington, 1773; Beecher and Brenowitz, 2005)
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