Anatomical traces of juvenile learning in the auditory system of adult barn owls

Abstract

Early experience plays a powerful role in shaping adult neural circuitry and behavior. In barn owls, early experience markedly influences sound localization. Juvenile owls that learn new, abnormal associations between auditory cues and locations in visual space as a result of abnormal visual experience can readapt to the same abnormal experience in adulthood, when plasticity is otherwise limited. Here we show that abnormal anatomical projections acquired during early abnormal sensory experience persist long after normal experience has been restored. These persistent projections are perfectly situated to provide a physical framework for subsequent readaptation in adulthood to the abnormal sensory conditions experienced in early life. Our results show that anatomical changes that support strong learned neural connections early in life can persist even after they are no longer functionally expressed. This maintenance of silenced neural circuitry that was once adaptive may represent an important mechanism by which the brain preserves a record of early experience.

Economic, Neurobiological and Behavioral Perspectives on Building America's Future Workforce

“…Similar structural changes have been observed in the visual cortex of kittens deprived of vision in one eye during a sensitive period (46). Once this additional circuitry is acquired and stabilized as a consequence of learning, it becomes highly resistant to elimination and can persist into adulthood (87). Owls that have learned an alternative map of auditory cues as juveniles can re-express that alternative map as adults should it become adaptive once again (Fig.…”

Vision Triggers an Experience-Dependent Sensitive Period at the Retinogeniculate Synapse

“…For example, anatomical changes in thalamocortical arbors occur after a week of monocular deprivation in cat (Antonini and Stryker, 1993), and anatomical changes in rodents are similarly delayed (Antonini et al, 1999) compared with the timing of physiological shifts in OD (Trachtenberg et al, 2000). Although the onset of plasticity may be slow, possibly reflecting the time for the structural reorganization of axon arbors, anatomical remnants of previously induced plasticity could result in more rapid changes during DR recovery (Linkenhoker et al, 2005;Hofer et al, 2006). In the cortex, dendrites are in close proximity to many potential partners but form synapses with only a subset (Shepherd et al, 2005), thus allowing the possibility for rapid connectivity changes without gross changes in arbors.…”

Perception in a Variable but Structured World: The Case of Speech Perception

“…a fear response or eyeblink) is not absolute, and the original conditioned association is still present and can re-appear under a variety of circumstances from re-introduction of the original context, very brief exposure to the conditioned association, or simply spontaneously (Thanellou & Green, 2011;Bouton & King, 1983;Sissons & R. R. Miller, 2009). Similarly, early exposure to perturbed audio-visual spatial correspondences in barn owls leads to more rapid re-adaptation to the same perturbation later in life, even with substantial un-perturbed experience in between (Körding, Tenenbaum, & Shadmehr, 2007;Knudsen, 1998;Linkenhoker et al, 2005). Similarly, talker-and group-specific expectations in speech perception could be seen as resulting from context-sensitive associative learning, although we have not described it as such.…”

“…Rather, by learning how statistical contingencies vary across contexts, you can take advantage of prior experience with a context when you next encounter it. Agents do, in fact, often encounter the same context repeatedly, and there is abundant evidence that when the context changes, learners do not forget old statistics (Thanellou & Green, 2011;Bouton & King, 1983;Sissons & R. R. Miller, 2009;Körding, Tenenbaum, & Shadmehr, 2007;Knudsen, 1998;Linkenhoker, von der Ohe, & Knudsen, 2005). A multi-context world thus requires inference at three levels.…”