Stimulus selection for gaze and spatial attention involves competition among stimuli across sensory modalities and across all of space. We demonstrate that such cross-modal, global competition takes place in the intermediate and deep layers of the optic tectum, a structure known to be involved in gaze control and attention. A variety of either visual or auditory stimuli located anywhere outside of a neuron's receptive field (RF) were shown to suppress or completely eliminate responses to a visual stimulus located inside the RF in nitrous oxide sedated owls. The essential mechanism underlying this stimulus competition is global, divisive inhibition. Unlike the effect of the classical inhibitory surround, which decreases with distance from the RF center and shapes neuronal responses to individual stimuli, global inhibition acts across the entirety of space and modulates responses primarily in the context of multiple stimuli. Whereas the source of this global inhibition is as yet unknown, our data indicate that different networks mediate the classical surround and global inhibition. We hypothesize that this global, cross-modal inhibition, which acts automatically in a bottom-up manner even in sedated animals, is critical to the creation of a map of stimulus salience in the optic tectum.

Essential to the selection of the next target for gaze or attention is the ability to compare the strengths of multiple competing stimuli (bottom-up information), and to signal the strongest one. Though the optic tectum (OT) has been causally implicated in stimulus selection, how it computes the strongest stimulus is unknown. Here, we demonstrate that OT neurons in the barn owl systematically encode the relative strengths of simultaneously occurring stimuli independently of sensory modality. Moreover, special “switch-like” responses of a subset of neurons abruptly increase when the stimulus inside their receptive field becomes the strongest one. Such responses are not predicted by responses to single stimuli and, indeed, are eliminated in the absence of competitive interactions. We demonstrate that this sensory transformation substantially boosts the representation of the strongest stimulus by creating a binary discrimination signal, thereby setting the stage for potential winner-take-all target selection for gaze and attention.

Interaural time differences are an important cue for azimuthal sound localization. It is still unclear whether the same neuronal mechanisms underlie the representation in the brain of interaural time difference in different vertebrates and whether these mechanisms are driven by common constraints, such as optimal coding. Current sound localization models may be discriminated by studying the spectral distribution of response peaks in tuning curves that measure the sensitivity to interaural time difference. The sound localization system of the barn owl has been studied intensively, but data that would allow discrimination between currently discussed models are missing from this animal. We have therefore obtained extracellular recordings from the time-sensitive subnuclei of the barn owl's inferior colliculus. Response peaks were broadly scattered over the physiological range of interaural time differences. A change in the representation of the interaural phase differences with frequency was not observed. In some neurons, response peaks fell outside the physiological range of interaural time differences. For a considerable number of neurons, the peak closest to zero interaural time difference was not the behaviorally relevant peak. The data are in best accordance with models suggesting that a place code underlies the representation of interaural time difference. The data from the high-frequency range, but not from the low-frequency range, are consistent with predictions of optimal coding. We speculate that the deviation of the representation of interaural time difference from optimal-coding models in the low-frequency range is attributable to the diminished importance of low frequencies for catching prey in this species.

The mechanisms by which the brain selects a particular stimulus as the next target for gaze are poorly understood. A cholinergic nucleus in the owl’s midbrain exhibits functional properties that suggest its role in bottom-up stimulus selection. Neurons in the nucleus isthmi pars parvocellularis (Ipc) respond to wide ranges of visual and auditory features, but they are not tuned to particular values of those features. Instead, they encode the relative strengths of stimuli across the entirety of space. Many neurons exhibit switch-like properties, abruptly increasing their responses to a stimulus in their receptive field when it becomes the strongest stimulus. This information propagates directly to the optic tectum, a structure involved in gaze control and stimulus selection, as periodic (25–50 Hz) bursts of cholinergic activity. The functional properties of Ipc neurons resemble those of a “salience map”, a core component in computational models for spatial attention and gaze control.

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