Auditory interneurons and sound localisation

The fact that a barn owl can localise sounds accurately under open-loop conditions implies that its auditory system can recognise each point in space from a unique combination of the cues that specify azimuth and elevation. Interneurons that respond to such complex combinations of stimulus features are found among higher-order neurons in the midbrain. The main auditory region of the midbrain in owls is situated on the inner edge of the optic tectum (Fig. 6.4a) and is divided functionally into an inner and

Figure 6.4 The neuronal map of auditory space in the midbrain of the barn owl. (a) The left side of the owl's brain, showing the location of the auditory midbrain (in bold outline) on the inner side of the optic tectum. (b) The left auditory midbrain enlarged from (a), with the co-ordinates of the neuronal map indicated in degrees of azimuth (L and R) and of elevation (+ and —) of auditory space. (c) A plot of auditory space in front of the owl in degrees of azimuth and of elevation, showing the receptive fields (bold rectangles) of ten neurons recorded in three separate electrode penetrations. The penetrations were made with the electrode parallel to the transverse plane at the positions indicated by the arrows linking (c) to (b). (Modified after Knudsen, 1981.)

Figure 6.4 The neuronal map of auditory space in the midbrain of the barn owl. (a) The left side of the owl's brain, showing the location of the auditory midbrain (in bold outline) on the inner side of the optic tectum. (b) The left auditory midbrain enlarged from (a), with the co-ordinates of the neuronal map indicated in degrees of azimuth (L and R) and of elevation (+ and —) of auditory space. (c) A plot of auditory space in front of the owl in degrees of azimuth and of elevation, showing the receptive fields (bold rectangles) of ten neurons recorded in three separate electrode penetrations. The penetrations were made with the electrode parallel to the transverse plane at the positions indicated by the arrows linking (c) to (b). (Modified after Knudsen, 1981.)

outer portion. In the inner portion, the interneurons are tuned to particular frequencies and are arranged according to their best frequency, which is termed a tonotopic arrangement. The great majority of these neurons respond to their best frequency regardless of where the sound source is located in space.

However, in the outer portion of the auditory midbrain, there are interneurons that respond quite differently; all have similar best frequencies near the upper end of the owl's range (6-8 kHz) and respond only when the sound originates from a specific region of space. These are therefore called space-specific neurons. When recording from such a neuron with a micro-electrode, the size and shape of the specific region to which it responds, termed the receptive field, can be determined with the movable speaker (Fig. 6.2a). Typically, the neuron is excited by sounds coming from a region of space shaped like a vertically elongated ellipse. Unlike most auditory neurons, the space-specific neurons are insensitive to changes in intensity, and even a 20 dB increase in intensity has little effect on the size of the receptive field.

As the recording electrode is advanced through the outer portion of the auditory midbrain, it samples neighbouring interneurons, which are found to have receptive fields representing neighbouring regions of space. In fact, the space-specific neurons are arranged systematically according to the azimuth and elevation of their receptive fields, so that they form a neuronal map of auditory space (Fig. 6.4b, c). Two-dimensional space is mapped on to the auditory midbrain, with azimuth being arrayed longitudinally and elevation being arrayed dorsoventrally. On each side of the brain, the map extends from 60° contralateral to 15° ipsilateral, but a disproportionately large number of neurons is devoted to the region between 15° contralateral and 15° ipsilateral. This arrangement means that the 30° of space directly in front of the owl is analysed by an especially large population of neurons on both sides of the brain. In elevation, the map extends from 40° upward to 80° downward but the majority of neurons are devoted to the region below the horizontal (Fig. 6.4c).

Partially blocking one ear, which changes the normal intensity differences between the ears, causes a significant vertical displacement of the receptive field in the space-specific neurons but makes little difference in azimuth. Changes in time differences between the ears can be delivered with the miniature earphones, and it is found that individual neurons respond only to a narrow range of time differences, which correspond with the horizontal location of the neuron's receptive field. Neurons that respond to small time differences have receptive fields in front of the face and those that respond to larger time differences have receptive fields at greater angles to the face. This shows that the azimuthal position of the receptive field is determined largely by time differences between the ears (Moiseff & Konishi, 1981).

Thus, the acoustic cues that are used to create the receptive fields of these auditory interneurons are exactly the same cues as the intact owl depends on for sound localisation. This fact makes it almost certain that the neuronal map of auditory space in the midbrain underlies the barn owl's skill in open-loop localisation. Certainly, the greater density of space-specific neurons devoted to the 30° arc in front of the face would account for the owl's greater accuracy in locating sounds in this region. The large proportion of the neuronal map that is devoted to the region of space somewhat below and in front of the face also makes good functional sense because this is likely to be the prey-containing region for an owl scanning the ground from its perch.

Barn owls normally use both sight and hearing to track their prey, and in keeping with this a combined auditory and visual map of space is found in the optic tectum. The auditory map in the tectum is derived by topographical projection from that in the auditory midbrain and is precisely aligned with the visual map of space derived from the retina. The mutual alignment is adjusted through sensory experience early in the life of the owl (Knudsen, 1983, 1998). In turn, this sensory map in the optic tectum is linked via neural circuits in the hindbrain to the motor circuits responsible for generating head movements (Masino & Knudsen, 1990).

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