Introduction

Visual and auditory information about the location of objects is processed and combined in a midbrain nucleus called the optic tectum (also called the superior colliculus [SC] in mammals). A primary function of the optic tectum is to create a multimodal map of space that can be used to orient attention and gaze toward interesting stimuli, regardless of the source of the sensory information (Peck, 1996; Stein & Meredith, 1993).

The optic tectum receives spatial information from the visual and auditory systems that is mutually independent and complementary. Vision provides high-resolution spatial information about the location of distant objects, even though they may be silent. Hearing provides spatial information about objects, even though they may not be visible. When objects can be both seen and heard, the cooperative combination of visual and auditory signals increases the capacity of the optic tectum to detect and locate stimuli under a wide range of difficult conditions (Stein & Meredith, 1993).

Combining spatial information across sensory modalities presents a challenging task to the nervous system, because visual and auditory information is initially encoded in completely different coordinate frames. Visual space is derived from the locus of activity within the topographic projections from the retina. In contrast, auditory space is derived from the evaluation of a variety of localization cues that arise from the interaction of incoming sound with the physical properties of the head and ears (Middlebrooks & Green, 1991). Auditory localization cues consist of interaural time differences (ITDs), which result from a difference in the distance traveled by a sound to reach the left versus the right ear, and interaural level differences (ILDs) and monaural spectral cues, both of which arise from the frequency-dependent directional properties of the external ears.

Visual and auditory spatial information is combined in the optic tectum by translating auditory cues into a topographic representation of space (Knudsen, 1982). The auditory system transforms its representations of cue values into a map of space by integrating information across frequency channels and across cues. This integration helps to resolve spatial ambiguities that are inherent to individual, frequency-specific cues and creates neurons that are broadly tuned for frequency but sharply tuned for space (Brainard, Knudsen, & Esterly, 1992). The auditory map is aligned with the visual map of space in the optic tectum so that tectal neurons respond to either visual or auditory stimuli located in the same region of space (Fig. 38.1).

Figure 38.1.  

Auditory and visual maps in the optic tectum. (A) Auditory and visual receptive fields measured from a bimodal unit in the optic tectum are plotted on a globe of space. The coordinates are relative to the visual axes of the owl. The visual receptive field, indicated by the circled V, was mapped by moving a light bar across the visual field. Responses of the unit to sound bursts (100 ms noise burst at 20 dB above threshold) as a function of azimuth and of elevation are shown below and to the right, respectively. The shaded area represents the area from which the sound response was more than 50% of maximum (auditory best area). (B) Lateral view of the left optic tectum. The contour lines indicate the locations of units with similar tuning. The approximate location of the recording site in A is indicated. C, contralateral; d, dorsal; r, rostral. (Adapted from Knudsen, 1982.)

The mutual alignment of visual and auditory receptive fields (RFs) in the tectum indicates that tectal neurons are tuned to the values of auditory cues that are produced by a sound source at the location of their visual RFs. Establishing and maintaining tuning to the correct values of auditory cues is made complicated by the variation in the correspondence between cue values and locations in the visual field that occurs across sound frequencies, across individuals, and within individuals during growth. Furthermore, the correspondence between encoded cue values and locations in the visual field changes with changes in the relative sensitivities of the ears and with development and aging of the nervous system. It is not surprising, therefore, that the tuning of tectal neurons to auditory localization cues is shaped by experience (King, Hutchings, Moore, & Blakemore, 1988; Knudsen & Knudsen, 1989; Knudsen, Knudsen, & Esterly, 1984).

This chapter discusses how visual experience shapes auditory tuning in the optic tectum. We focus on data from the barn owl because its auditory map exhibits the highest resolution among all species studied, and our knowledge of the effects of experience on the map is most complete for this species. We describe mechanisms of adaptive auditory plasticity and the teaching signals that guide the plasticity. Finally, we present a model that accounts for the plasticity in terms of cellular mechanisms and principles of learning that are likely to apply equally well to other species and to other networks in the brain.