Age reduces the brain's ability to adapt to change. But a surprising measure of neural adaptation does occur, at least in one experimental situation, if change is introduced bit by bit.
They say that you can't teach an old dog new tricks. But on page 293 of this issue1 Linkenhoker and Knudsen provide evidence that you can at least teach an old owl new tricks — if you train it in small steps. This result implies that the brains of older animals, including ourselves, may be capable of greater change in the form of adaptive plasticity than previously expected.
Owls are nocturnal hunters which rely on auditory as well as visual information to track their prey. Coordinated maps of auditory and visual space are formed in the optic tectum, the midbrain region responsible for orienting the owl to its target2. The visual map is essentially a direct representation of information from the retina, but the auditory map results from a more complex computation, based in part on the microsecond differences between the time of arrival of sounds at each ear. For proper coordination of its auditory and visual worlds, the young owl must learn, for instance, that when it is looking directly at a mouse, the mouse's terrified squeak reaches both ears at the same time. But when the squeak reaches the right ear first by a certain number of microseconds, the owl should expect to see the mouse a certain number of degrees to the right.
Experiments with juvenile birds have shown that visual information has the upper hand in maintaining the coordination between these two maps. In such birds, Knudsen and a colleague3 previously found that an optical shift of the visual world, achieved by placing prism glasses on the owls, results in a gradual shift of the auditory map to keep sight and sound coordinated. This plasticity may seem somewhat maladaptive under the conditions of the experiment — that is, although it is the visual world that has changed the visual map stays the same. However, it implies that outside the laboratory, over the course of evolution, vision has proven to be the more accurate and reliable indicator of spatial location for guiding orienting behaviours.
Although adaptive adjustments in the brain's representation of the auditory world occur with relative ease in juvenile birds, it was thought that adult owls were less malleable in this respect (Fig. 1). The same prisms placed on an older owl, even for a period of months, cause only a tiny shift of the auditory map. In line with the terminology used in other kinds of neural systems, this window for large-scale auditory–visual realignment might be called a 'critical period' in development.
Evidence for critical periods in neural development dates back to the classic experiments of Hubel and Wiesel4, who deprived kittens of visual input to one eye and then showed that the animals' binocular vision, as well as the responses of their visual-cortex cells, differed from those of kittens raised normally. But identical manipulation of visual information had no effect in older cats. Other familiar examples of critical periods include language acquisition in humans and song learning by certain birds5. Critical periods in cognitive development are the rationale for playing Mozart to babies.
Linkenhoker and Knudsen1 now show that the auditory map in older owls does indeed cope poorly with a large shift of the visual world. However, by shifting the visual world gradually, in several small steps, the map achieves a much greater degree of adaptive change than was previously believed possible. If, instead of being exposed to a single prismatic shift of 23°, older owls were first exposed sequentially to shifts of 6°, 11° and 17°, they acquired new auditory maps that could be reproduced by subsequent exposure to a single large prismatic shift.
These results by no means overturn the principle of a critical period. The auditory maps in juvenile owls adjust to much larger changes, and to about twice the extent, compared with adult owls. However, these findings do challenge us to be more precise in defining what is meant by a critical period. They also challenge the notion that the same training regimes should be used when assessing adult and juvenile capacities for neural plasticity. Although there are striking parallels between the mechanisms of plastic change that operate during development and in adulthood, it is by no means clear that they will be the same, even within one system. A better understanding of the neural mechanisms underlying this form of plasticity in adult owls should lead to a better grasp of the limits of, and capacities for, adult learning.
There is some evidence that the degree of plasticity in this system may be limited by the extent of branching of the relevant neuronal elements, which seems to shrink as the owl matures. Knudsen's group6 has shown that large prismatic shifts can induce adaptive change in the auditory maps of adult owls that had previously adapted to the same large shifts as juveniles. This suggests that learning during the juvenile period causes some neuroanatomical or neurochemical foundation to be laid down in these animals that enables the signal for change to manifest itself over a much wider range than would otherwise be seen in the adult. It is tempting to think that the training regime used in the current experiments was more successful because it was working within the constraints of more refined neural architecture that could bootstrap a more gradual, progressive change.
Finally, it should be noted that these experiments were done in laboratory owls that weren't really doing what owls like to do best with their orienting behaviours — hunt for prey. The plasticity measured here is in terms of days and weeks of experience, rather than, for instance, the number of practice trials, which is often considered the important variable in perceptual learning experiments in humans. An owl whose survival depends on successfully orienting to its prey may display an even greater capacity for change, for instance by virtue of neuromodulatory systems that become engaged during such 'arousing' activities as hunting. Whatever the case, these experiments should offer the hope to those of us who aren't getting any younger that improving learning ability just means finding new strategies for inducing plasticity in our brains.
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Doupe, A. J. & Kuhl, P. K. Annu. Rev. Neurosci. 22, 567–631 (1999).
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