Direction Specific Biases in Human Visual and Vestibular Heading Perception

The adaptive plasticity of the spatial organization of the vestibuloocular reflex (VOR) has been investigated in intact and canal-plugged primates using 2-h exposure to conflicting visual (optokinetic, OKN) and vestibular rotational stimuli about mutually orthogonal axes (generating torsional VOR + vertical OKN, torsional VOR + horizontal OKN, vertical VOR + horizontal OKN, and horizontal VOR + vertical OKN). Adaptation protocols with 0.5-Hz (+/-18 degrees ) head movements about either an earth-vertical or an earth-horizontal axis induced orthogonal response components as high as 40-70% of those required for ideal adaptation. Orthogonal response gains were highest at the adapting frequency with phase leads present at lower and phase lags present at higher frequencies. Furthermore, the time course of adaptation, as well as orthogonal response dynamics were similar and relatively independent of the particular visual/vestibular stimulus combination. Low-frequency (0. 05 Hz, vestibular stimulus: +/-60 degrees ; optokinetic stimulus: +/-180 degrees ) adaptation protocols with head movements about an earth-vertical axis induced smaller orthogonal response components that did not exceed 20-40% of the head velocity stimulus (i.e., approximately 10% of that required for ideal adaptation). At the same frequency, adaptation with head movements about an earth-horizontal axis generated large orthogonal responses that reached values as high as 100-120% of head velocity after 2 h of adaptation (i.e., approximately 40% of ideal adaptation gains). The particular spatial and temporal response characteristics after low-frequency, earth-horizontal axis adaptation in both intact and canal-plugged animals strongly suggests that the orienting (and perhaps translational) but not inertial (velocity storage) components of the primate otolith-ocular system exhibit spatial adaptability. Due to the particular nested arrangement of the visual and vestibular stimuli, the optic flow pattern exhibited a significant component about the third spatial axis (i.e., orthogonal to the axes of rotation of the head and visual surround) at twice the oscillation frequency. Accordingly, the adapted VOR was characterized consistently by a third response component (orthogonal to both the axes of head and optokinetic drum rotation) at twice the oscillation frequency after earth-horizontal but not after earth-vertical axis 0.05-Hz adaptation. This suggests that the otolith-ocular (but not the semicircular canal-ocular) system can adaptively change its spatial organization at frequencies different from those of the head movement.

Responses to visual, acoustic, and vestibular stimuli were studied in neurons of the middle and deep layers of the tectum in the pigeon. Changes in the receptive field (RF) were assessed from comparison of unit responses to isolated movement of a shaped visual stimulus with responses to movement of a stimulus during simultaneous action of a vestibular or acoustic stimulus. Changes in RF of the neuron could be observed during the action of both a vestibular and an acoustic stimulus. These changes affected the identification of the predominant direction of movement of the stimulus, the position of the maximum in the response histogram, and the duration and number of spikes in the response. The direction of change in RF of the neuron was found not necessarily to coincide with the sign of the response to the same neuron to isolated presentation of a vestibular or acoustic stimulus. It is postulated on the basis of the results and data in the literature that the tectum transforms the flow of impulses arriving from the retina depending on the nature of the information received by it from other sensory systems.

Detection of asymmetries has been a mainstay of using vestibular reflexes to assess semicircular canal function. However, there has been relatively little work on how vestibular stimuli are perceived. Suprathreshold vestibular perception was measured in 13 normal healthy controls by having them compare the relative sizes of two yaw (vertical-axis rotation) or sway (right-left translation) stimuli. Both stimuli were 1.5 s in duration with a staircase used to adjust the relative size of the stimuli to find a pair of stimuli perceived as equal. Motion stimuli were delivered in darkness using a hexapod motion platform, and visual stimuli simulating motion were presented on a screen in the absence of platform motion. Both same direction (SD) and opposite direction (OD) stimuli were delivered in separate runs. After a two-interval stimulus, subjects reported which movement they perceived as larger. Cumulative distribution functions were fit to the responses so that the relative magnitudes of the two stimuli perceived as equal could be determined. For OD trial blocks, a directional asymmetry index was calculated to compare the relative size of perceived rightward and leftward motion. For all trial blocks, a temporal asymmetry index (TAI) was used to compare the relative size of the first and second intervals. Motion OD stimuli were perceived as equal in all subjects in yaw and all but one in sway. For visual OD stimuli, two subjects had slightly asymmetric responses for both sway and yaw. The TAI demonstrated asymmetry in 54% in yaw, in which the second interval was perceived to be larger in all but one subject who had an asymmetry. For sway, only two subjects had a significant asymmetry. Visual stimuli produced a similar rate of asymmetry. The direction and magnitude of these asymmetries were not significantly correlated with those seen for motion stimuli. Asymmetries were found in a fraction with the TAI in SD stimuli for motion in yaw (42%) and sway (33%), as well as for vision in yaw (60%) and sway (43%). The precision at discriminating SD motion stimuli decreased significantly with age, but there was no difference in OD motion or visual stimuli.

A moving visual field can induce the feeling of self-motion or vection. Illusory motion from static repeated asymmetric patterns creates a compelling visual motion stimulus, but it is unclear if such illusory motion can induce a feeling of self-motion or alter self-motion perception. In these experiments, human subjects reported the perceived direction of self-motion for sway translation and yaw rotation at the end of a period of viewing set visual stimuli coordinated with varying inertial stimuli. This tested the hypothesis that illusory visual motion would influence self-motion perception in the horizontal plane. Trials were arranged into 5 blocks based on stimulus type: moving star field with yaw rotation, moving star field with sway translation, illusory motion with yaw, illusory motion with sway, and static arrows with sway. Static arrows were used to evaluate the effect of cognitive suggestion on self-motion perception. Each trial had a control condition; the illusory motion controls were altered versions of the experimental image, which removed the illusory motion effect. For the moving visual stimulus, controls were carried out in a dark room. With the arrow visual stimulus, controls were a gray screen. In blocks containing a visual stimulus there was an 8s viewing interval with the inertial stimulus occurring over the final 1s. This allowed measurement of the visual illusion perception using objective methods. When no visual stimulus was present, only the 1s motion stimulus was presented. Eight women and five men (mean age 37) participated. To assess for a shift in self-motion perception, the effect of each visual stimulus on the self-motion stimulus (cm/s) at which subjects were equally likely to report motion in either direction was measured. Significant effects were seen for moving star fields for both translation (p = 0.001) and rotation (p<0.001), and arrows (p = 0.02). For the visual motion stimuli, inertial motion perception was shifted in the direction consistent with the visual stimulus. Arrows had a small effect on self-motion perception driven by a minority of subjects. There was no significant effect of illusory motion on self-motion perception for either translation or rotation (p>0.1 for both). Thus, although a true moving visual field can induce self-motion, results of this study show that illusory motion does not.

How multisensory cues affect processing in early sensory brain areas is not well understood. The inferior colliculus (IC) is an early auditory structure that is visually responsive (Porter KK, Metzger RR, Groh JM. Proc Natl Acad Sci USA 104: 17855-17860, 2007; Bulkin DA, Groh JM. Front Neural Circuits 6: 61, 2012; Bulkin DA, Groh JM. J Neurophysiol 107: 785-795, 2012), but little is known about how visual signals affect the IC's auditory representation. We explored how visual cues affect both spiking and local field potential (LFP) activity in the IC of two monkeys performing a task involving saccades to auditory, visual, or combined audiovisual stimuli. We confirm that LFPs are sensitive to the onset of fixation lights and the onset of visual targets presented during steady fixation. The LFP waveforms evoked by combined audiovisual stimuli differed from those evoked by sounds alone. In single-unit spiking activity, responses were weak when visual stimuli were presented alone, but visual stimuli could modulate the activity evoked by sounds in a stronger way. Such modulations could involve either increases or decreases in activity, and whether increases or decreases were observed was variable and not obviously correlated with the responses evoked by visual or auditory stimuli alone. These findings indicate that visual stimuli shape the IC's auditory representation in flexible ways that differ from those observed previously in multisensory areas.NEW & NOTEWORTHY We find that the inferior colliculus, a primarily auditory brain area, displays distinct population-level responses to visual stimuli. We also find that visual cues can influence the auditory responses of individual neurons. Together, the results provide insight into how relatively early sensory areas may play a role in combining multiple sensory modalities to refine the perception of complex environments.

Sensory processing disturbance in autistic children as a predictor of response to sensory integrative procedures was investigated. Ten autistic children, ages 3-1/2 to 13 years (mean, 7.4 years), were initially evaluated in regard to their hypo-, hyper-, or normal responsivity to visual, auditory, tactile, vestibular, proprioceptive, olfactory, and gustatory stimuli. After evaluation, each child received therapy that provided somatosensory and vestibular stimulation and elicited adaptive responses to these stimuli. At the end of one year of therapy, each child's progress was judged in relationship to that of the others, and the group was divided into the six best and the four poorest respondents. Stepwise discriminant analysis identified which initial test variables predicted good or poor responses to therapy. The good respondents showed tactile defensiveness, avoidance of movement, gravitational insecurity, and an orienting response to an air puff. Results suggest that children who registered sensory input but failed to modulate it responded better to therapy than those who were hypo-responsive or failed to orient to sensory input.

Increased visual task difficulty enhances attentional capture by both visual and auditory distractor stimuli

Heading estimation involves both inertial and visual cues. Inertial motion is sensed by the labyrinth, somatic sensation by the body, and optic flow by the retina. Because the eye and head are mobile these stimuli are sensed relative to different reference frames and it remains unclear if a perception occurs in a common reference frame. Recent neurophysiologic evidence has suggested the reference frames remain separate even at higher levels of processing but has not addressed the resulting perception. Seven human subjects experienced a 2s, 16 cm/s translation and/or a visual stimulus corresponding with this translation. For each condition 72 stimuli (360° in 5° increments) were delivered in random order. After each stimulus the subject identified the perceived heading using a mechanical dial. Some trial blocks included interleaved conditions in which the influence of ±28° of gaze and/or head position were examined. The observations were fit using a two degree-of-freedom population vector decoder (PVD) model which considered the relative sensitivity to lateral motion and coordinate system offset. For visual stimuli gaze shifts caused shifts in perceived head estimates in the direction opposite the gaze shift in all subjects. These perceptual shifts averaged 13 ± 2° for eye only gaze shifts and 17 ± 2° for eye-head gaze shifts. This finding indicates visual headings are biased towards retina coordinates. Similar gaze and head direction shifts prior to inertial headings had no significant influence on heading direction. Thus inertial headings are perceived in body-centered coordinates. Combined visual and inertial stimuli yielded intermediate results.

Introduction One of the most common approaches in individuals with unilateral peripheral vestibular dysfunction (UPVD) is vestibular rehabilitation (RV). Many factors can negatively affect the result of RV. Virtual reality based treatment may represent an important tool in the solution of these problems. In individuals with UPVD there is a decrease in the reception of vestibular stimuli and there is an adjustment in the reception of visual and proprioceptive stimuli. They use more visual cues to minimise the decrease in vestibular stimuli – visual dependence (VD). Although the importance and results of virtual reality as a tool in improving balance in individuals with UPVD have already been demonstrated, we intend to demonstrate that virtual reality allows significant improvements in the decrease in VD. Objectives The aim of the study is to compare VD levels in individuals with UPVD after RV program by virtual reality. Methodology For the evaluation of VD, dynamic posturography was performed with the Balance Rehabilition Unit equipment for 39 people with UPVD, before and after the RV program by virtual reality. Ten conditions were tested, with different visual and propriocetive stimuli. The parameters considered were the oscillation area of the pressure centre and the sway velocity. Results In the parameter of the oscillation area of the pressure centre, statistically significant results were found in the 10 conditions tested. In the sway velocity parameter, statistically significant results were found in the condition 1, 2, 3, 4, 5 e 10. Conclusion Virtual reality incorporated in the RV programs presents itself as an important tool in improving VD in individuals with UPVD.

Selective Engagement of Plasticity Mechanisms for Motor Memory Storage

Decision letter: Visual and motor signatures of locomotion dynamically shape a population code for feature detection in Drosophila

Heading estimation is vital to everyday navigation and locomotion. Despite extensive behavioral and physiological research on both visual and vestibular heading estimation over more than two decades, the accuracy of heading estimation has not yet been systematically evaluated. Therefore human visual and vestibular heading estimation was assessed in the horizontal plane using a motion platform and stereo visual display. Heading angle was overestimated during forward movements and underestimated during backward movements in response to both visual and vestibular stimuli, indicating an overall multimodal bias toward lateral directions. Lateral biases are consistent with the overrepresentation of lateral preferred directions observed in neural populations that carry visual and vestibular heading information, including MSTd and otolith afferent populations. Due to this overrepresentation, population vector decoding yields patterns of bias remarkably similar to those observed behaviorally. Lateral biases are inconsistent with standard Bayesian accounts which predict that estimates should be biased toward the most common straight forward heading direction. Nevertheless, lateral biases may be functionally relevant. They effectively constitute a perceptual scale expansion around straight ahead which could allow for more precise estimation and provide a high gain feedback signal to facilitate maintenance of straight-forward heading during everyday navigation and locomotion.

Multisensory integration is a powerful mechanism for maximizing sensitivity to sensory events. We examined its effects on auditory localization in healthy human subjects. The specific objective was to test whether the relative intensity and location of a seemingly irrelevant visual stimulus would influence auditory localization in accordance with the inverse effectiveness and spatial rules of multisensory integration that have been developed from neurophysiological studies with animals [Stein and Meredith, 1993 The Merging of the Senses (Cambridge, MA: MIT Press)]. Subjects were asked to localize a sound in one condition in which a neutral visual stimulus was either above threshold (supra-threshold) or at threshold. In both cases the spatial disparity of the visual and auditory stimuli was systematically varied. The results reveal that stimulus salience is a critical factor in determining the effect of a neutral visual cue on auditory localization. Visual bias and, hence, perceptual translocation of the auditory stimulus appeared when the visual stimulus was supra-threshold, regardless of its location. However, this was not the case when the visual stimulus was at threshold. In this case, the influence of the visual cue was apparent only when the two cues were spatially coincident and resulted in an enhancement of stimulus localization. These data suggest that the brain uses multiple strategies to integrate multisensory information.

The effect of visual task difficulty and attentional direction on the detection of acoustic change as indexed by the Mismatch Negativity

Since the advent of functional magnetic resonance imaging cognitive science has experienced a turn towards neuroscience. Models of perceptual and cognitive functions can now be tested against patterns of human brain activity in anatomically well-defined regions of interest. Structural and functional connectivity analyses can inform us about how different brain regions are interconnected and interact in perceptual and cognitive tasks, as well as during resting states. In this study I review the results of a series of experiments that aimed to reveal the visual-vestibular sensory processing underlying self-motion perception. We (Frank, Baumann, Mattingley, & Greenlee, 2014; Frank, Wirth, & Greenlee, 2016) localized regions in the posterior insula using fMRI with visual and vestibular stimuli. The results suggest that two areas in this part of the brain are involved in self-motion perception: the parieto-insular vestibular cortex (PIVC) for the processing of vestibular information and posterior insular cortex (PIC) for the integration of visual and vestibular information. The results suggest that these two regions play different roles in the integration of visual and vestibular cues related to self-motion perception.