The inferior colliculus (IC) is a major processing center situated mid-way along both the ascending and descending auditory pathways of the brain stem. Although it is fundamentally an auditory area, the IC also receives anatomical input from non-auditory sources. Neurophysiological studies corroborate that non-auditory stimuli can modulate auditory processing in the IC and even elicit responses independent of coincident auditory stimulation. In this article, we review anatomical and physiological evidence for multisensory and other non-auditory processing in the IC. Specifically, the contributions of signals related to vision, eye movements and position, somatosensation, and behavioral context to neural activity in the IC will be described. These signals are potentially important for localizing sound sources, attending to salient stimuli, distinguishing environmental from self-generated sounds, and perceiving and generating communication sounds. They suggest that the IC should be thought of as a node in a highly interconnected sensory, motor, and cognitive network dedicated to synthesizing a higher-order auditory percept rather than simply reporting patterns of air pressure detected by the cochlea. We highlight some of the potential pitfalls that can arise from experimental manipulations that may disrupt the normal function of this network, such as the use of anesthesia or the severing of connections from cortical structures that project to the IC. Finally, we note that the presence of these signals in the IC has implications for our understanding not just of the IC but also of the multitude of other regions within and beyond the auditory system that are dependent on signals that pass through the IC. Whatever the IC "hears" would seem to be passed both "upward" to thalamus and thence to auditory cortex and beyond, as well as "downward" via centrifugal connections to earlier areas of the auditory pathway such as the cochlear nucleus.
The inferior colliculus (IC) is an essential stop early in the ascending auditory pathway. Though normally thought of as a predominantly auditory structure, recent work has uncovered a variety of non-auditory influences on firing rate in the IC. Here, we map the location within the IC of neurons that respond to the onset of a fixation-guiding visual stimulus. Visual/visuomotor associated activity was found throughout the IC (overall, 84 of 199 sites tested or 42%), but with a far reduced prevalence and strength along recording penetrations passing through the tonotopically organized region of the IC, putatively the central nucleus (11 of 42 sites tested, or 26%). These results suggest that visual information has only a weak effect on early auditory processing in core regions, but more strongly targets the modulatory shell regions of the IC.
Visual and auditory spatial signals initially arise in different reference frames. It has been postulated that auditory signals are translated from a head-centered to an eye-centered frame of reference compatible with the visual spatial maps, but, to date, only various forms of hybrid reference frames for sound have been identified. Here, we show that the auditory representation of space in the superior colliculus involves a hybrid reference frame immediately after the sound onset but evolves to become predominantly eye centered, and more similar to the visual representation, by the time of a saccade to that sound. Specifically, during the first 500 ms after the sound onset, auditory response patterns (N = 103) were usually neither head nor eye centered: 64% of neurons showed such a hybrid pattern, whereas 29% were more eye centered and 8% were more head centered. This differed from the pattern observed for visual targets (N = 156): 86% were eye centered,
The inferior colliculus (IC) is thought to have two main subdivisions, a central region that forms an important stop on the ascending auditory pathway and a surrounding shell region that may play a more modulatory role. In this study, we investigated whether eye position affects activity in both the central and shell regions. Accordingly, we mapped the location of eye position-sensitive neurons in six monkeys making spontaneous eye movements by sampling multiunit activity at regularly spaced intervals throughout the IC. We used a functional map based on auditory response patterns to estimate the anatomical location of recordings, in conjunction with structural MRI and histology. We found eye position-sensitive sites throughout the IC, including at 27% of sites in tonotopically organized recording penetrations (putatively the central nucleus). Recordings from surrounding tissue showed a larger proportion of sites indicating an influence of eye position (33-43%). When present, the magnitude of the change in activity due to eye position was often comparable to that seen for sound frequency. Our results indicate that the primary ascending auditory pathway is influenced by the position of the eyes. Because eye position is essential for visual-auditory integration, our findings suggest that computations underlying visual-auditory integration begin early in the ascending auditory pathway.
The inferior colliculus (IC) is thought to have two main subdivisions, a central region that forms an important stop on the ascending auditory pathway and a surrounding shell region that may play a more modulatory role. In this study, we investigated whether eye position affects activity in both the central and shell regions. Accordingly, we mapped the location of eye position sensitive neurons in 6 monkeys making spontaneous eye movements by sampling multi-unit activity at regularly spaced intervals throughout the IC. We used a functional map based on auditory response patterns to estimate the anatomical location of recordings, in conjunction with structural MRI and histology. We found eye position sensitive sites throughout the IC, including at 27% of sites in tonotopically organized recording penetrations (putatively the central nucleus). Recordings from surrounding tissue showed a larger proportion of sites showing an influence of eye position (33-43%). When present, the magnitude of the change in activity due to eye position could be comparable to that seen for sound frequency. Our results indicate that the primary ascending auditory pathway is influenced by the position of the eyes. Because eye position is essential for visual-auditory integration, our findings suggest that computations underlying visual-auditory integration begin early in the ascending auditory pathway.
We investigated the functional architecture of the inferior colliculus (IC) in rhesus monkeys. We systematically mapped multiunit responses to tonal stimuli and noise in the IC and surrounding tissue of six rhesus macaques, collecting data at evenly placed locations and recording nonresponsive locations to define boundaries. The results show a modest tonotopically organized region (17 of 100 recording penetration locations in 4 of 6 monkeys) surrounded by a large mass of tissue that, although vigorously responsive, showed no clear topographic arrangement (68 of 100 penetration locations). Rather, most cells in these recordings responded best to frequencies at the low end of the macaque auditory range. The remaining 15 (of 100) locations exhibited auditory responses that were not sensitive to sound frequency. Potential anatomical correlates of functionally defined regions and implications for midbrain auditory prosthetic devices are discussed.
The motor layers of the superior colliculus (SC) are thought to specify saccade amplitude and direction, independent of initial eye position. However, recent evidence suggests that eye position can modulate the level of activity of SC motor neurons. In this study, we tested whether initial eye position has an effect on microstimulation-evoked saccade amplitude. High (>300 Hz) and low (
We evaluated to what extent the influence of eye position in the auditory pathway of primates can be described as a gain field. We compared single unit activity in the inferior colliculus (IC), core auditory cortex (A1) and the caudomedial belt (CM) region of auditory cortex (AC) in primates, and found stronger evidence for gain field-like interactions in the IC than in AC. In the IC, eye position signals showed both multiplicative and additive interactions with auditory responses, whereas in AC the effects were not as well predicted by a gain field model.
The motor layers of the superior colliculus (SC) are thought to specify saccade amplitude and direction, independent of initial eye position. However, recent evidence suggests that eye position can modulate the level of activity of SC motor neurons. In this study, we tested whether initial eye position has an effect on microstimulation-evoked saccade amplitude. High (>300 Hz) and low (
We use both vision and audition when localizing objects and events in our environment. However, these sensory systems receive spatial information in different coordinate systems: sounds are localized using inter-aural and spectral cues, yielding a head-centered representation of space, whereas the visual system uses an eye-centered representation of space, based on the site of activation on the retina. In addition, the visual system employs a place-coded, retinotopic map of space, whereas the auditory system's representational format is characterized by broad spatial tuning and a lack of topographical organization. A common view is that the brain needs to reconcile these differences in order to control behavior, such as orienting gaze to the location of a sound source. To accomplish this, it seems that either auditory spatial information must be transformed from a head-centered rate code to an eye-centered map to match the frame of reference used by the visual system, or vice versa. Here, we review a number of studies that have focused on the neural basis underlying such transformations in the primate auditory system. Although, these studies have found some evidence for such transformations, many differences in the way the auditory and visual system encode space exist throughout the auditory pathway. We will review these differences at the neural level, and will discuss them in relation to differences in the way auditory and visual information is used in guiding orienting movements.
Seeing the image of a newscaster on a television set causes us to think that the sound coming from the loudspeaker is actually coming from the screen. How images capture sounds is mysterious because the brain uses different methods for determining the locations of visual versus auditory stimuli. The retina senses the locations of visual objects with respect to the eyes, whereas differences in sound characteristics across the ears indicate the locations of sound sources referenced to the head. Here, we tested which reference frame (RF) is used when vision recalibrates perceived sound locations. Visually guided biases in sound localization were induced in seven humans and two monkeys who made eye movements to auditory or audiovisual stimuli. On audiovisual (training) trials, the visual component of the targets was displaced laterally by 5-6 degrees. Interleaved auditory-only (probe) trials served to evaluate the effect of experience with mismatched visual stimuli on auditory localization. We found that the displaced visual stimuli induced ventriloquism aftereffect in both humans (approximately 50% of the displacement size) and monkeys (approximately 25%), but only for locations around the trained spatial region, showing that audiovisual recalibration can be spatially specific. We tested the reference frame in which the recalibration occurs. On probe trials, we varied eye position relative to the head to dissociate head- from eye-centered RFs. Results indicate that both humans and monkeys use a mixture of the two RFs, suggesting that the neural mechanisms involved in ventriloquism occur in brain region(s) using a hybrid RF for encoding spatial information.
The reference frame used by intraparietal cortex neurons to encode locations is controversial. Many previous studies have suggested eye-centered coding, whereas we have reported that visual and auditory signals employ a hybrid reference frame (i.e., a combination of head- and eye-centered information) (Mullette-Gillman et al. 2005). One possible explanation for this discrepancy is that sensory-related activity, which we studied previously, is hybrid, whereas motor-related activity might be eye centered. Here, we examined the reference frame of visual and auditory saccade-related activity in the lateral and medial banks of the intraparietal sulcus (areas lateral intraparietal area [LIP] and medial intraparietal area [MIP]) of 2 rhesus monkeys. We recorded from 275 single neurons as monkeys performed visual and auditory saccades from different initial eye positions. We found that both visual and auditory signals reflected a hybrid of head- and eye-centered coordinates during both target and perisaccadic task periods rather than shifting to an eye-centered format as the saccade approached. This account differs from numerous previous recording studies. We suggest that the geometry of the receptive field sampling in prior studies was biased in favor of an eye-centered reference frame. Consequently, the overall hybrid nature of the reference frame was overlooked because the non-eye-centered response patterns were not fully characterized.
Is sound location represented in the auditory cortex of humans and monkeys? Human neuroimaging experiments have had only mixed success at demonstrating sound location sensitivity in primary auditory cortex. This is in apparent conflict with studies in monkeys and other animals, in which single-unit recording studies have found stronger evidence for spatial sensitivity. Does this apparent discrepancy reflect a difference between humans and animals, or does it reflect differences in the sensitivity of the methods used for assessing the representation of sound location? The sensitivity of imaging methods such as functional magnetic resonance imaging depends on the following two key aspects of the underlying neuronal population: (1) what kind of spatial sensitivity individual neurons exhibit and (2) whether neurons with similar response preferences are clustered within the brain. To address this question, we conducted a single-unit recording study in monkeys. We investigated the nature of spatial sensitivity in individual auditory cortical neurons to determine whether they have receptive fields (place code) or monotonic (rate code) sensitivity to sound azimuth. Second, we tested how strongly the population of neurons favors contralateral locations. We report here that the majority of neurons show predominantly monotonic azimuthal sensitivity, forming a rate code for sound azimuth, but that at the population level the degree of contralaterality is modest. This suggests that the weakness of the evidence for spatial sensitivity in human neuroimaging studies of auditory cortex may be attributable to limited lateralization at the population level, despite what may be considerable spatial sensitivity in individual neurons.
The reference frame used by intraparietal cortex neurons to encode locations is controversial. Many previous studies have suggested eye-centered coding, whereas we have reported that visual and auditory signals employ a hybrid reference frame (i.e., a combination of head- and eye-centered information) (Mullette-Gillman et al. 2005). One possible explanation for this discrepancy is that sensory-related activity, which we studied previously, is hybrid, whereas motor-related activity might be eye centered. Here, we examined the reference frame of visual and auditory saccade-related activity in the lateral and medial banks of the intraparietal sulcus (areas lateral intraparietal area [LIP] and medial intraparietal area [MIP]) of 2 rhesus monkeys. We recorded from 275 single neurons as monkeys performed visual and auditory saccades from different initial eye positions. We found that both visual and auditory signals reflected a hybrid of head- and eye-centered coordinates during both target and perisaccadic task periods rather than shifting to an eye-centered format as the saccade approached. This account differs from numerous previous recording studies. We suggest that the geometry of the receptive field sampling in prior studies was biased in favor of an eye-centered reference frame. Consequently, the overall hybrid nature of the reference frame was overlooked because the non-eye-centered response patterns were not fully characterized.
The inferior colliculus (IC) is normally thought of as a predominantly auditory structure because of its early position in the ascending auditory pathway just before the auditory thalamus. Here, we show that a majority of IC neurons (64% of 180 neurons) in awake monkeys carry visual- and/or saccade-related signals in addition to their auditory responses (P
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How the brain responds to sequences of sounds is a question of great relevance to a variety of auditory perceptual phenomena. We investigated how long the responses of neurons in the primary auditory cortex of awake monkeys are influenced by the previous sound. We found that responses to the second sound of a two-sound sequence were generally attenuated compared to the response that sound evoked when it was presented first. The attenuation remained evident at the population level even out to inter-stimulus intervals (ISIs) of 5 s, although it was of modest size for ISIs >2 s. Behavioral context (performance versus non-performance of a visual fixation task during sound presentation) did not influence the results. The long time course of the first sound's influence suggests that, under natural conditions, neural responses in auditory cortex are rarely governed solely by the current sound
When you hear a salient sound, it is natural to look at it to find out what is happening. Orienting the eyes to look at sounds is essential to our ability to identify and understand the events occurring in our environment. This behavior involves both sensorimotor and multisensory integration: a sound elicits a movement of the visual sense organ, the eye, to bring the source of the sound under visual scrutiny. How are auditory signals converted into oculomotor commands? This chapter describes our recent work concerning the necessary computational steps between sound and eye movement, and how they may be implemented in neural populations in the primate brain.
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