Audio-Visual Integration in a Redundant Target Paradigm: A Comparison between Rhesus Macaque and Man.

The mechanisms underlying multi-sensory interactions are still poorly understood despite considerable progress made since the first neurophysiological recordings of multi-sensory neurons. While the majority of single-cell neurophysiology has been performed in anesthetized or passive-awake laboratory animals, the vast majority of behavioral data stems from studies with human subjects. Interpretation of neurophysiological data implicitly assumes that laboratory animals exhibit perceptual phenomena comparable or identical to those observed in human subjects. To explicitly test this underlying assumption, we here characterized how two rhesus macaques and four humans detect changes in intensity of auditory, visual, and audio-visual stimuli. These intensity changes consisted of a gradual envelope modulation for the sound, and a luminance step for the LED. Subjects had to detect any perceived intensity change as fast as possible. By comparing the monkeys' results with those obtained from the human subjects we found that (1) unimodal reaction times differed across modality, acoustic modulation frequency, and species, (2) the largest facilitation of reaction times with the audio-visual stimuli was observed when stimulus onset asynchronies were such that the unimodal reactions would occur at the same time (response, rather than physical synchrony), and (3) the largest audio-visual reaction-time facilitation was observed when unimodal auditory stimuli were difficult to detect, i.e., at slow unimodal reaction times. We conclude that despite marked unimodal heterogeneity, similar multisensory rules applied to both species. Single-cell neurophysiology in the rhesus macaque may therefore yield valuable insights into the mechanisms governing audio-visual integration that may be informative of the processes taking place in the human brain.

Hearing aid fitting for visual and hearing impaired patients with Usher syndrome type IIa.

OBJECTIVES: Usher syndrome is the leading cause of hereditary deaf-blindness. Most patients with Usher syndrome type IIa start using hearing aids from a young age. A serious complaint refers to interference between sound localisation abilities and adaptive sound processing (compression), as present in today's hearing aids. The aim of this study was to investigate the effect of advanced signal processing on binaural hearing, including sound localisation. DESIGN AND PARTICIPANTS: In this prospective study, patients were fitted with hearing aids with a nonlinear (compression) and linear amplification programs. Data logging was used to objectively evaluate the use of either program. Performance was evaluated with a speech-in-noise test, a sound localisation test and two questionnaires focussing on self-reported benefit. RESULTS: Data logging confirmed that the reported use of hearing aids was high. The linear program was used significantly more often (average use: 77%) than the nonlinear program (average use: 17%). The results for speech intelligibility in noise and sound localisation did not show a significant difference between type of amplification. However, the self-reported outcomes showed higher scores on 'ease of communication' and overall benefit, and significant lower scores on disability for the new hearing aids when compared to their previous hearing aids with compression amplification. CONCLUSIONS: Patients with Usher syndrome type IIa prefer a linear amplification over nonlinear amplification when fitted with novel hearing aids. Apart from a significantly higher logged use, no difference in speech in noise and sound localisation was observed between linear and nonlinear amplification with the currently used tests. Further research is needed to evaluate the reasons behind the preference for the linear settings.

Blink perturbation effects on saccades evoked by microstimulation of the superior colliculus.

Current knowledge of saccade-blink interactions suggests that blinks have paradoxical effects on saccade generation. Blinks suppress saccade generation by attenuating the oculomotor drive command in structures like the superior colliculus (SC), but they also disinhibit the saccadic system by removing the potent inhibition of pontine omnipause neurons (OPNs). To better characterize these effects, we evoked the trigeminal blink reflex by delivering an air puff to one eye as saccades were evoked by sub-optimal stimulation of the SC. For every stimulation site, the peak and average velocities of stimulation with blink movements (SwBMs) were lower than stimulation-only saccades (SoMs), supporting the notion that the oculomotor drive is weakened in the presence of a blink. In contrast, the duration of the SwBMs was longer, consistent with the hypothesis that the blink-induced inhibition of the OPNs could prolong the window of time available for oculomotor commands to drive an eye movement. The amplitude of the SwBM could also be larger than the SoM amplitude obtained from the same site, particularly for cases in which blink-associated eye movements exhibited the slowest kinematics. The results are interpreted in terms of neural signatures of saccade-blink interactions.

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus.

A major challenge in computational neurobiology is to understand how populations of noisy, broadly-tuned neurons produce accurate goal-directed actions such as saccades. Saccades are high-velocity eye movements that have stereotyped, nonlinear kinematics; their duration increases with amplitude, while peak eye-velocity saturates for large saccades. Recent theories suggest that these characteristics reflect a deliberate strategy that optimizes a speed-accuracy tradeoff in the presence of signal-dependent noise in the neural control signals. Here we argue that the midbrain superior colliculus (SC), a key sensorimotor interface that contains a topographically-organized map of saccade vectors, is in an ideal position to implement such an optimization principle. Most models attribute the nonlinear saccade kinematics to saturation in the brainstem pulse generator downstream from the SC. However, there is little data to support this assumption. We now present new neurophysiological evidence for an alternative scheme, which proposes that these properties reside in the spatial-temporal dynamics of SC activity. As predicted by this scheme, we found a remarkably systematic organization in the burst properties of saccade-related neurons along the rostral-to-caudal (i.e., amplitude-coding) dimension of the SC motor map: peak firing-rates systematically decrease for cells encoding larger saccades, while burst durations and skewness increase, suggesting that this spatial gradient underlies the increase in duration and skewness of the eye velocity profiles with amplitude. We also show that all neurons in the recruited population synchronize their burst profiles, indicating that the burst-timing of each cell is determined by the planned saccade vector in which it participates, rather than by its anatomical location. Together with the observation that saccade-related SC cells indeed show signal-dependent noise, this precisely tuned organization of SC burst activity strongly supports the notion of an optimal motor-control principle embedded in the SC motor map as it fully accounts for the straight trajectories and kinematic nonlinearity of saccades.

A test of spatial temporal decoding mechanisms in the superior colliculus.

Population coding is a ubiquitous principle in the nervous system for the proper control of motor behavior. A significant amount of research is dedicated to studying population activity in the superior colliculus (SC) to investigate the motor control of saccadic eye movements. Vector summation with saturation (VSS) has been proposed as a mechanism for how population activity in the SC can be decoded to generate saccades. Interestingly, the model produces different predictions when decoding two simultaneous populations at high vs. low levels of activity. We tested these predictions by generating two simultaneous populations in the SC with high or low levels of dual microstimulation. We also combined varying levels of stimulation with visually induced activity. We found that our results did not perfectly conform to the predictions of the VSS scheme and conclude that the simplest implementation of the model is incomplete. We propose that additional parameters to the model might account for the results of this investigation.

Linear visuomotor transformations in midbrain superior colliculus control saccadic eye-movements.

It is well established that a localized population of neurons in the motor map of the midbrain superior colliculus (SC) drives a saccadic eye-head gaze shift. However, there is controversy as to how the brainstem saccade burst generators decode the SC activity. We focus on eye-movement generation by comparing two competing schemes from the recent literature that are both supported by neurophysiological evidence: the vector-averaging scheme versus the vector summation model. Whereas the former contains at least four nonlinearities to explain visuomotor planning and saccade execution, the latter relies predominantly on linear operations. We have demonstrated that the summation model accounts for the nonlinear main sequence of saccade kinematics, and predicted that this results from a spatial gradient in temporal burst profiles of SC cells: rostral cells have higher peak-firing rates and shorter burst durations than caudal cells. Yet, the number of spikes in their saccade-related bursts is identical. In contrast, the averaging model does not predict such activity profiles. We now also show that by incorporating the concept of predictive remapping in the spatial updating of saccade sequences, the phenomenon of target averaging in double-stimulation experiments, and the occurrence of goal-directed, but highly curved saccades in the double-step paradigm, can all be explained by the same linear summation mechanism. We argue that the linear model is more in line with neurophysiological data, while relying on fewer ad-hoc assumptions than the nonlinear vector-averaging scheme.

Differential effects of reflex blinks on saccade perturbations in humans.

Studies in both humans and monkeys have indicated that blinks affect the central programming of saccades. In this study, we compared the influence of two types of reflex blinks on the trajectories and kinematics of memory-guided saccades in human subjects. We found that electrical stimulation of the supraorbital nerve shortly before or during a saccade briefly halts or decelerates the eye in midflight. After this short interruption, the eye always resumed its course and reached the target location in the absence of visual feedback. Air puff stimuli produced significant decreases in mean eye velocity too, but in addition to these changes in saccade kinematics, they produced much larger and more variable perturbations of the two-dimensional saccade trajectories. Even so, the endpoints of blink-perturbed saccades obtained under both test conditions remained as accurate and as precise as those observed in the control condition. We hypothesize that the reduction in mean eye velocity is not caused by a trigeminal reactivation of brain stem omnipause neurons but could instead arise from a trigeminal transient inhibition of saccade-related activity in the midbrain superior colliculus (SC). These findings support the theory that blink-perturbed saccades are programmed as slow, but straight, saccades onto which blink-related eye movements are superimposed. This linear superposition occurs downstream from the SC.

Linear ensemble-coding in midbrain superior colliculus specifies the saccade kinematics.

Recently, we proposed an ensemble-coding scheme of the midbrain superior colliculus (SC) in which, during a saccade, each spike emitted by each recruited SC neuron contributes a fixed minivector to the gaze-control motor output. The size and direction of this 'spike vector' depend exclusively on a cell's location within the SC motor map (Goossens and Van Opstal, in J Neurophysiol 95: 2326-2341, 2006). According to this simple scheme, the planned saccade trajectory results from instantaneous linear summation of all spike vectors across the motor map. In our simulations with this model, the brainstem saccade generator was simplified by a linear feedback system, rendering the total model (which has only three free parameters) essentially linear. Interestingly, when this scheme was applied to actually recorded spike trains from 139 saccade-related SC neurons, measured during thousands of eye movements to single visual targets, straight saccades resulted with the correct velocity profiles and nonlinear kinematic relations ('main sequence properties' and 'component stretching'). Hence, we concluded that the kinematic nonlinearity of saccades resides in the spatial-temporal distribution of SC activity, rather than in the brainstem burst generator. The latter is generally assumed in models of the saccadic system. Here we analyze how this behaviour might emerge from this simple scheme. In addition, we will show new experimental evidence in support of the proposed mechanism.

Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus.

Performance in a reaction time task can be strongly influenced by the physical properties of the stimuli used (e.g., position and intensity). The reduction in reaction time observed with higher-intensity visual stimuli has been suggested to arise from reduced processing time along the visual pathway. If this hypothesis is correct, activity should be registered in neurons sooner for higher-intensity stimuli. We evaluated this hypothesis by measuring the onset of neural activity in the intermediate layers of the superior colliculus while monkeys generated saccades to high or low-intensity visual stimuli. When stimulus intensity was high, the response onset latency was significantly reduced compared to low-intensity stimuli. As a result, the minimum time for visually triggered saccades was reduced, accounting for the shorter saccadic reaction times (SRTs) observed following high-intensity stimuli. Our results establish a link between changes in neural activity related to stimulus intensity and changes to SRTs, which supports the hypothesis that shorter SRTs with higher-intensity stimuli are due to reduced processing time.

Dynamic ensemble coding of saccades in the monkey superior colliculus.

The deeper layers of the midbrain superior colliculus (SC) contain a topographic motor map in which a localized population of cells is recruited for each saccade, but how the brain stem decodes the dynamic SC output is unclear. Here we analyze saccade-related responses in the monkey SC to test a new dynamic ensemble-coding model, which proposes that each spike from each saccade-related SC neuron adds a fixed, site-specific contribution to the intended eye movement command. As predicted by this simple theory, we found that the cumulative number of spikes in the cell bursts is tightly related to the displacement of the eye along the ideal straight trajectory, both for normal saccades and for strongly curved, blink-perturbed saccades toward a single visual target. This dynamic relation depends systematically on the metrics of the saccade displacement vector, and can be fully predicted from a quantitative description of the cell's classical movement field. Furthermore, we show that a linear feedback model of the brain stem, which is driven by dynamic linear vector summation of measured SC firing patterns, produces realistic two-dimensional (2D) saccade trajectories and kinematics. We conclude that the SC may act as a nonlinear, vectorial saccade generator that programs an optimal straight eye-movement trajectory.

Auditory-visual interactions subserving goal-directed saccades in a complex scene.

This study addresses the integration of auditory and visual stimuli subserving the generation of saccades in a complex scene. Previous studies have shown that saccadic reaction times (SRTs) to combined auditory-visual stimuli are reduced when compared with SRTs to either stimulus alone. However, these results have been typically obtained with high-intensity stimuli distributed over a limited number of positions in the horizontal plane. It is less clear how auditory-visual interactions influence saccades under more complex but arguably more natural conditions, when low-intensity stimuli are embedded in complex backgrounds and distributed throughout two-dimensional (2-D) space. To study this problem, human subjects made saccades to visual-only (V-saccades), auditory-only (A-saccades), or spatially coincident auditory-visual (AV-saccades) targets. In each trial, the low-intensity target was embedded within a complex auditory-visual background, and subjects were allowed over 3 s to search for and foveate the target at 1 of 24 possible locations within the 2-D oculomotor range. We varied systematically the onset times of the targets and the intensity of the auditory target relative to background [i.e., the signal-to-noise (S/N) ratio] to examine their effects on both SRT and saccadic accuracy. Subjects were often able to localize the target within one or two saccades, but in about 15% of the trials they generated scanning patterns that consisted of many saccades. The present study reports only the SRT and accuracy of the first saccade in each trial. In all subjects, A-saccades had shorter SRTs than V-saccades, but were more inaccurate than V-saccades when generated to auditory targets presented at low S/N ratios. AV-saccades were at least as accurate as V-saccades but were generated at SRTs typical of A-saccades. The properties of AV-saccades depended systematically on both stimulus timing and S/N ratio of the auditory target. Compared with unimodal A- and V-saccades, the improvements in SRT and accuracy of AV-saccades were greatest when the visual target was synchronous with or leading the auditory target, and when the S/N ratio of the auditory target was lowest. Further, the improvements in saccade accuracy were greater in elevation than in azimuth. A control experiment demonstrated that a portion of the improvements in SRT could be attributable to a warning-cue mechanism, but that the improvements in saccade accuracy depended on the spatial register of the stimuli. These results agree well with earlier electrophysiological results obtained from the midbrain superior colliculus (SC) of anesthetized preparations, and we argue that they demonstrate multisensory integration of auditory and visual signals in a complex, quasi-natural environment. A conceptual model incorporating the SC is presented to explain the observed data.

Two-dimensional sound-localization behavior of early-blind humans.

To investigate whether the visual system is crucial for adequate calibration of acoustic localization cues, sound-localization performance of early blind humans was compared with that of sighted controls. Because a potential benefit of vision is mainly expected for targets within the two-dimensional (2D) frontal hemifield, localization was tested within this target range, while using sounds of various durations and spectral content. Subjects were instructed to point, in separate experimental sessions, either with their left arm, or with their nose, in the direction of the perceived target position as accurately as possible. The experiments required the use of all available sound-localization cues such as interaural differences in phase and intensity, as well as the complex spectral shape cues provided by the pinnae. In addition, for long-duration stimuli, subjects could have had access to head motion-induced acoustic feedback. Moreover, the two pointing methods allowed us to assess different response strategies for the two groups. In an additional series, subjects were instructed to respond as quickly as possible. The results show that, in general, 2D sound-localization performance of blind subjects was indistinguishable from that of sighted subjects, both for broad-band noise and for pure tones. In the fast head-pointing task, the latency distributions of both groups were equal. These findings suggest that visual feedback is not required to calibrate the available localization cues--including the idiosyncratic and complex spectral shape cues for elevation. Instead, the localization abilities of blind people show that the putative supervising role of vision may be supported, or taken over, by other non-visual feedback systems. The results do not provide support for the hypothesis that blind people can hypercompensate for the loss of vision in the frontal hemifield by developing superior sound-localization abilities. Despite the general correspondence in localization behavior, some specific differences related to pointing strategies as well as to those between blind and sighted subjects were apparent. Most importantly, the reconstructed origin (bias) of arm pointing was located near the shoulder for the blind subjects, whereas it was shifted and located near the cyclopean eye for the sighted subjects. The results indicate that both early blind and sighted humans adequately transform the head-centered acoustic target coordinates into the required reference frame of either motor system, but that the adopted response strategy may be specific to the subject group and pointer method.

A spatial hearing deficit in early-blind humans.

An important issue in neuroscience is the effect of visual loss on the remaining senses. Two opposing views have been advanced. On the one hand, visual loss may lead to compensatory plasticity and sharpening of the remaining senses. On the other hand, early blindness may also prevent remaining sensory modalities from a full development. In the case of sound localization, it has been reported recently that, under certain conditions, early-blind humans can localize sounds better than sighted controls. However, these studies were confined to a single sound source in the horizontal plane. This study compares sound localization of early-blind and sighted subjects in both the horizontal and vertical domain, whereas background noise was added to test more complex hearing conditions. The data show that for high signal-to-noise (S/N) ratios, localization by blind and sighted subjects is similar for both azimuth and elevation. At decreasing S/N ratios, the accuracy of the elevation response components deteriorated earlier than the accuracy of the azimuth component in both subject groups. However, although azimuth performance was identical for the two groups, elevation accuracy deteriorated much earlier in the blind subject group. These results indicate that auditory hypercompensation in early-blind humans does not extend to the frontal target domain, where the potential benefit of vision is maximal. Moreover, the results demonstrate for the first time that in this domain the human auditory system may require vision to optimally calibrate the elevation-related spectral pinna cues. Sensitivity to azimuth-encoding binaural difference cues, however, may be adequately calibrated in the absence of vision.

Blink-perturbed saccades in monkey. I. Behavioral analysis.

Saccadic eye movements are thought to be influenced by blinking through premotor interactions, but it is still unclear how. The present paper describes the properties of blink-associated eye movements and quantifies the effect of reflex blinks on the latencies, metrics, and kinematics of saccades in the monkey. In particular, it is examined to what extent the saccadic system accounts for blink-related perturbations of the saccade trajectory. Trigeminal reflex blinks were elicited near the onset of visually evoked saccades by means of air puffs directed on the eye. Reflex blinks were also evoked during a straight-ahead fixation task. Eye and eyelid movements were measured with the magnetic-induction technique. The data show that saccade latencies were reduced substantially when reflex blinks were evoked prior to the impending visual saccades as if these saccades were triggered by the blink. The evoked blinks also caused profound spatial-temporal perturbations of the saccades. Deflections of the saccade trajectory, usually upward, extended up to approximately 15 degrees. Saccade peak velocities were reduced, and a two- to threefold increase in saccade duration was typically observed. In general, these perturbations were largely compensated in saccade mid-flight, despite the absence of visual feedback, yielding near-normal endpoint accuracies. Further analysis revealed that blink-perturbed saccades could not be described as a linear superposition of a pure blink-associated eye movement and an unperturbed saccade. When evoked during straight-ahead fixation, blinks were accompanied by initially upward and slightly abducting eye rotations of approximately 2-15 degrees. Back and forth wiggles of the eye were frequently seen; but in many cases the return movement was incomplete. Rather than drifting back to its starting position, the eye then maintained its eccentric orbital position until a downward corrective saccade toward the fixation spot followed. Blink-associated eye movements were quite rapid, albeit slower than saccades, and the velocity-amplitude-duration characteristics of the initial excursions as well as the return movements were approximately linear. These data strongly support the idea that blinks interfere with the saccade premotor circuit, presumably upstream from the neural eye-position integrator. They also indicated that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensatory behavior. The tight latency coupling between saccades and blinks is consistent with an inhibition of omnipause neurons by the blink system, suggesting that the observed changes in saccade kinematics arise elsewhere in the saccadic premotor system.

Blink-perturbed saccades in monkey. II. Superior colliculus activity.

Trigeminal reflex blinks evoked near the onset of a saccade cause profound spatial-temporal perturbations of the saccade that are typically compensated in mid-flight. This paper investigates the influence of reflex blinks on the discharge properties of saccade-related burst neurons (SRBNs) in intermediate and deep layers of the monkey superior colliculus (SC). Twenty-nine SRBNs, recorded in three monkeys, were tested in the blink-perturbation paradigm. We report that the air puff stimuli, used to elicit blinks, resulted in a short-latency ( approximately 10 ms) transient suppression of saccade-related SRBN activity. Shortly after this suppression (within 10-30 ms), all neurons resumed their activity, and their burst discharge then continued until the perturbed saccade ended near the extinguished target. This was found regardless whether the compensatory movement was into the cell's movement field or not. In the limited number of trials where no compensation occurred, the neurons typically stopped firing well before the end of the eye movement. Several aspects of the saccade-related activity could be further quantified for 25 SRBNs. It appeared that 1) the increase in duration of the high-frequency burst was well correlated with the (two- to threefold) increase in duration of the perturbed movement. 2) The number of spikes in the burst for control and perturbed saccades was quite similar. On average, the number of spikes increased only 14%, whereas the mean firing rate in the burst decreased by 52%. 3) An identical number of spikes were obtained between control and perturbed responses when burst and postsaccadic activity were both included in the spike count. 4) The decrease of the mean firing rate in the burst was well correlated with the decrease in the velocity of perturbed saccades. 5) Monotonic relations between instantaneous firing rate and dynamic motor error were obtained for control responses but not for perturbed responses. And 6) the high-frequency burst of SRBNs with short-lead and long-lead presaccadic activity (also referred to as burst and buildup neurons, respectively) showed very similar features. Our findings show that blinking interacts with the saccade premotor system already at the level of the SC. The data also indicate that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensation for blink-related perturbations. We propose that these interactions occur downstream from the motor SC and that the latter may encode the desired displacement vector of the eyes by sending an approximately fixed number of spikes to the brainstem saccadic burst generator.

Influence of head position on the spatial representation of acoustic targets.

Sound localization in humans relies on binaural differences (azimuth cues) and monaural spectral shape information (elevation cues) and is therefore the result of a neural computational process. Despite the fact that these acoustic cues are referenced with respect to the head, accurate eye movements can be generated to sounds in complete darkness. This ability necessitates the use of eye position information. So far, however, sound localization has been investigated mainly with a fixed head position, usually straight ahead. Yet the auditory system may rely on head motor information to maintain a stable and spatially accurate representation of acoustic targets in the presence of head movements. We therefore studied the influence of changes in eye-head position on auditory-guided orienting behavior of human subjects. In the first experiment, we used a visual-auditory double-step paradigm. Subjects made saccadic gaze shifts in total darkness toward brief broadband sounds presented before an intervening eye-head movement that was evoked by an earlier visual target. The data show that the preceding displacements of both eye and head are fully accounted for, resulting in spatially accurate responses. This suggests that auditory target information may be transformed into a spatial (or body-centered) frame of reference. To further investigate this possibility, we exploited the unique property of the auditory system that sound elevation is extracted independently from pinna-related spectral cues. In the absence of such cues, accurate elevation detection is not possible, even when head movements are made. This is shown in a second experiment where pure tones were localized at a fixed elevation that depended on the tone frequency rather than on the actual target elevation, both under head-fixed and -free conditions. To test, in a third experiment, whether the perceived elevation of tones relies on a head- or space-fixed target representation, eye movements were elicited toward pure tones while subjects kept their head in different vertical positions. It appeared that each tone was localized at a fixed, frequency-dependent elevation in space that shifted to a limited extent with changes in head elevation. Hence information about head position is used under static conditions too. Interestingly, the influence of head position also depended on the tone frequency. Thus tone-evoked ocular saccades typically showed a partial compensation for changes in static head position, whereas noise-evoked eye-head saccades fully compensated for intervening changes in eye-head position. We propose that the auditory localization system combines the acoustic input with head-position information to encode targets in a spatial (or body-centered) frame of reference. In this way, accurate orienting responses may be programmed despite intervening eye-head movements. A conceptual model, based on the tonotopic organization of the auditory system, is presented that may account for our findings.

Visual-auditory interactions modulate saccade-related activity in monkey superior colliculus.

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.

Spectro-temporal factors in two-dimensional human sound localization.

This paper describes the effect of spectro-temporal factors on human sound localization performance in two dimensions (2D). Subjects responded with saccadic eye movements to acoustic stimuli presented in the frontal hemisphere. Both the horizontal (azimuth) and vertical (elevation) stimulus location were varied randomly. Three types of stimuli were used, having different spectro-temporal patterns, but identically shaped broadband averaged power spectra: noise bursts, frequency-modulated tones, and trains of short noise bursts. In all subjects, the elevation components of the saccadic responses varied systematically with the different temporal parameters, whereas the azimuth response components remained equally accurate for all stimulus conditions. The data show that the auditory system does not calculate a final elevation estimate from a long-term (order 100 ms) integration of sensory input. Instead, the results suggest that the auditory system may apply a "multiple-look" strategy in which the final estimate is calculated from consecutive short-term (order few ms) estimates. These findings are incorporated in a conceptual model that accounts for the data and proposes a scheme for the temporal processing of spectral sensory information into a dynamic estimate of sound elevation.

Relearning sound localization with new ears.

Because the inner ear is not organized spatially, sound localization relies on the neural processing of implicit acoustic cues. To determine a sound's position, the brain must learn and calibrate these cues, using accurate spatial feedback from other sensorimotor systems. Experimental evidence for such a system has been demonstrated in barn owls, but not in humans. Here, we demonstrate the existence of ongoing spatial calibration in the adult human auditory system. The spectral elevation cues of human subjects were disrupted by modifying their outer ears (pinnae) with molds. Although localization of sound elevation was dramatically degraded immediately after the modification, accurate performance was steadily reacquired. Interestingly, learning the new spectral cues did not interfere with the neural representation of the original cues, as subjects could localize sounds with both normal and modified pinnae.

Local feedback signals are not distorted by prior eye movements: evidence from visually evoked double saccades.

Recent experiments have shown that the amplitude and direction of saccades evoked by microstimulation of the monkey superior colliculus depend systematically on the amplitude and direction of preceding visually guided saccades as well as on the postsaccade stimulation interval. The data are consistent with the hypothesis that an eye displacement integrator in the local feedback loop of the saccadic burst generator is gradually reset with a time constant of approximately 45 ms. If this is true, similar effects should occur during naturally evoked saccade sequences, causing systematic interval-dependent errors. To test this prediction in humans, saccades toward visual single- and double-step stimuli were elicited, and the properties of the second saccades were investigated as a function of the intersaccadic interval (ISI). In 15-20% of the saccadic responses, ISIs fell well below 100 ms. The errors of the second saccades were not systematically affected by the preceding primary saccade, irrespective of the ISI. Only a slight increase in the endpoint variability of second saccades was observed for the shortest ISIs. These results are at odds with the hypothesis that the putative eye displacement integrator has a reset time constant >10 ms. Instead, it is concluded that the signals involved in the internal feedback control of the saccadic burst generator reflect eye position and/or eye displacement accurately, irrespective of preceding eye movements.