Hearing and looking.

Many objects in the real world have multiple sensory attributes—for example, an object may both reflect light and emit sound. This leads to the percept that both the sound and the light originate from the same object, even though the neural processing of spatial information by the visual and auditory system is very different. In the visual system, space is encoded at the level of the retina based on the position of the activated photoreceptors. Thus, visual space must initially be represented in an eye-centered reference frame. In the auditory system, spatial information must be computed based on differences in intensity and timing of the stimulus at the two ears and on spectral cues resulting from reflections of the stimulus by the torso, head, and pinnae. Thus, since the ears are fixed to the head, auditory spatial information should be represented in a head-centered reference frame. At some point in the nervous system, these two reference frames must somehow align in order to create the unified percept of a single object.A central question is what reference frame(s) the nervous system uses to encode the spatial attributes of single- and multimodal stimuli and how these reference frames could be used to generate unified percepts. Several studies have investigated how the position of an auditory stimulus relative to the head and to the eyes modulates neuronal responses in multimodal regions of the brain (see Andersen, 1997xAndersen, R.A. Phil. Trans. R. Soc. Lond. B. 1997; 352: 1421–1428Crossref | PubMed | Scopus (263)See all ReferencesAndersen, 1997). For example, in the parietal lobe (Stricanne et al., 1996xStricanne, B., Andersen, R.A., and Mazzoni, P. J. Neurophysiol. 1996; 76: 2071–2076PubMedSee all References)(Stricanne et al., 1996) and the superior colliculus (Jay and Sparks, 1987xJay, M.F. and Sparks, D.L. J. Neurophysiol. 1987; 57: 35–55PubMedSee all References)(Jay and Sparks, 1987), the responses of neurons to auditory stimuli are modulated by the eye position, so most of these neurons do not represent space in a purely head-centered reference frame. What has not been carefully examined is how early in the processing pathway that the reference frame of auditory neurons can be modulated.The results from experiments tackling this issue are reported by Groh et al. (2001)xGroh, J.M., Trause, A.S., Underhill, A.M., Clark, K.R., and Inati, S. Neuron. 2001; 29: 509–518Abstract | Full Text | Full Text PDF | PubMed | Scopus (108)See all References)Groh et al. (2001) in this issue of Neuron. They measured the responses of single neurons to noise stimuli in the inferior colliculus while monkeys were either looking to the left, to the right, or straight ahead (see Figure 1Figure 1, left column). The inferior colliculus has traditionally been considered a “relay” nucleus, in which inputs from the auditory brainstem converge and are then relayed to the thalamus. One would therefore expect these neurons to encode acoustic space in a head-centered reference frame (see Figure 1Figure 1, middle column), and not an eye-centered reference frame (see Figure 1Figure 1, right column). Groh et al. (2001)xGroh, J.M., Trause, A.S., Underhill, A.M., Clark, K.R., and Inati, S. Neuron. 2001; 29: 509–518Abstract | Full Text | Full Text PDF | PubMed | Scopus (108)See all References)Groh et al. (2001) found that approximately one-third of the neurons encountered showed neither a head-centered nor an eye-centered reference frame, but something in between.Figure 1Head-Centered versus Eye-Centered Reference FramesThe left column shows a schematic of the types of trials used in the experiments by Groh et al. (2001)xGroh, J.M., Trause, A.S., Underhill, A.M., Clark, K.R., and Inati, S. Neuron. 2001; 29: 509–518Abstract | Full Text | Full Text PDF | PubMed | Scopus (108)See all References)Groh et al. (2001). In this example, the speaker located directly in front of the monkey emits a noise stimulus, but the monkey may be fixating on a visual target to the left (top, green lines), directly ahead (middle, blue lines), or to the right (bottom, red lines). For each cell, all auditory locations were tested with the monkey fixating each of these three different targets. The plots in the right two columns show the expected results depending on whether the neuron's reference frame is head-centered (left) or eye-centered (right). Each colored line represents the neural response when the monkey is fixating at one of the three locations and is plotted as a function of the auditory stimulus location relative to the orientation of the head (top two plots); the same data are replotted centered on the fixation point (bottom two plots). For a head-centered reference frame, the three colored lines should be superimposed when plotted with respect to the head. When plotted with respect to the fixation point, in this example, the neuron would have the greatest response to the right of the fixation point when the monkey is looking toward the left, and the reverse when the monkey is looking toward the right. If the neuron responded in an eye-centered reference frame, the opposite would be true. Groh et al. (2001)xGroh, J.M., Trause, A.S., Underhill, A.M., Clark, K.R., and Inati, S. Neuron. 2001; 29: 509–518Abstract | Full Text | Full Text PDF | PubMed | Scopus (108)See all References)Groh et al. (2001) found something between these twoView Large Image | View Hi-Res Image | Download PowerPoint SlideThis result indicates that the visual system can influence auditory spatial processing at a very early level and raises several interesting questions. How is the eye position information incorporated in the responses of inferior collicular neurons? How does eye position influence the spatial processing of other auditory areas such as the thalamus and cortex? Is it the strategy of the nervous system to encode spatial information across all sensory modalities in a similar reference frame as soon as possible? Investigating these questions should provide key insights into general mechanisms of sensory representations and perception.