Hunting increases adaptive auditory map plasticity in adult barn owls

Abstract

The optic tectum (OT) of barn owls contains topographic maps of auditory and visual space. Barn owls reared with horizontally displacing prismatic spectacles (prisms) acquire a novel auditory space map in the OT that restores alignment with the prismatically displaced visual map. Although juvenile owls readily acquire alternative maps of auditory space as a result of experience, this plasticity is reduced greatly in adults. We tested whether hunting live prey, a natural and critically important behavior for barn owls, increases auditory map plasticity in adult owls. Two groups of naive adult owls were fit with prisms. The first group was fed dead mice during 10 weeks of prism experience, while the second group was required to hunt live prey for an identical period of time. When the owls hunted live prey, auditory maps shifted substantially farther (five times farther, on average) and the consistency of tuning curve shifts within each map increased. Only a short period of time in each day, during which the two groups experienced different conditions, accounts for this effect. In addition, increased map plasticity correlated with behavioral improvements in the owls' ability to strike and capture prey. These results indicate that the experience of hunting dramatically increases adult adaptive plasticity in this pathway.

Figure 1.

Effect of prism experience with and without hunting on ITD tuning in the OT of an adult barn owl. A, C, and E are raster displays of multiunit responses to a range of ITD values for single recording sites. The values are relative to the value predicted from the location of the visual receptive field for each site (see Materials and Methods). Time is measured relative to stimulus onset, and the duration of the stimulus is indicated by the bar at the bottom. Negative ITDs designate left-ear leading ITDs. The arrows on the right indicate the ITD value that was instructed by prism experience. B, D, and F are ITD tuning curves derived from data such as shown on the left for all of the sites sampled in this bird. Thin lines are curves from individual sites; thick lines are population averages. Arrows indicate the ITD value that was instructed by prisms.

Figure 2.

Effect of hunting on auditory plasticity in adult barn owls. A, The average map shift in the OT of 12 barn owls. The three left bars represent data from a group of seven owls before prism experience, after prism experience, and after prism experience with hunting (left to right). The extreme right bar represents data from a second group of five owls exposed immediately to hunting with prisms. The maximum expected shift, based on the visual displacement of the prisms, is indicated by the horizontal line at 42.5 μs. The map shift of each individual bird is indicated for each condition (short horizontal marks). B, The map shift ± SEM that follows prism experience with and without hunting for the four birds for which both conditions were tested. The magnitude of shifts in the hunting and nonhunting conditions was correlated negatively, indicating that larger map shifts induced in the nonhunting condition decreased subsequent shifts to prisms of the opposite direction during the hunting condition (linear regression; r² = 0.94; p < 0.05).

Figure 3.

Average map shift of individual owls as a function of the change in strike success. The diagonal line represents the linear correlation of improvement in strike success (final strike success - initial strike success) with the magnitude of auditory map plasticity (r² = 0.90; p < 0.05). Error bars for both strike success and map shift are the 95% confidence intervals on the measurements.