The activity of sensory neural populations carries information about the environment. This may be extracted from neural activity using different strategies. In the auditory brainstem, a recent theory proposes that sound location in the horizontal plane is decoded from the relative summed activity of two populations in each hemisphere, whereas earlier theories hypothesized that the location was decoded from the identity of the most active cells. We tested the performance of various decoders of neural responses in increasingly complex acoustical situations, including spectrum variations, noise, and sound diffraction. We demonstrate that there is insufficient information in the pooled activity of each hemisphere to estimate sound direction in a reliable way consistent with behavior, whereas robust estimates can be obtained from neural activity by taking into account the heterogeneous tuning of cells. These estimates can still be obtained when only contralateral neural responses are used, consistently with unilateral lesion studies.
Having two ears allows animals to localize the source of a sound. For example, barn owls can snatch their prey in complete darkness by relying on sound alone. It has been known for a long time that this ability depends on tiny differences in the sounds that arrive at each ear, including differences in the time of arrival: in humans, for example, sound will arrive at the ear closer to the source up to half a millisecond earlier than it arrives at the other ear. These differences are called interaural time differences. However, the way that the brain processes this information to figure out where the sound came from has been the source of much debate.
Several theories have been proposed for how the brain calculates position from interaural time differences. According to the hemispheric theory, the activities of particular binaurally sensitive neurons in each of side of the brain are added together: adding signals in this way has been shown to maximize sensitivity to time differences under simple, controlled circumstances. The peak decoding theory proposes that the brain can work out the location of a sound on the basis of which neurons responded most strongly to the sound.
Both theories have their potential advantages, and there is evidence in support of each. Now, Goodman et al. have used computational simulations to compare the models under ecologically relevant circumstances. The simulations show that the results predicted by both models are inconsistent with those observed in real animals, and they propose that the brain must use the full pattern of neural responses to calculate the location of a sound.
One of the parts of the brain that is responsible for locating sounds is the inferior colliculus. Studies in cats and humans have shown that damage to the inferior colliculus on one side of the brain prevents accurate localization of sounds on the opposite side of the body, but the animals are still able to locate sounds on the same side. This finding is difficult to explain using the hemispheric model, but Goodman et al. show that it can be explained with pattern-based models.