Detection thresholds of macaque otolith afferents

The vestibular system is our sixth sense and is important for spatial perception functions, yet the sensory detection and discrimination properties of vestibular neurons remain relatively unexplored. Here we have used signal detection theory to measure detection thresholds of otolith afferents using 1 Hz linear accelerations delivered along three cardinal axes. Direction detection thresholds were measured by comparing mean firing rates centered on response peak and trough (full-cycle thresholds) or by comparing peak/trough firing rates with spontaneous activity (half-cycle thresholds). Thresholds were similar for utricular and saccular afferents, as well as for lateral, fore/aft, and vertical motion directions. When computed along the preferred direction, full-cycle direction detection thresholds were 7.54 and 3.01 cm/s(2) for regular and irregular firing otolith afferents, respectively. Half-cycle thresholds were approximately double, with excitatory thresholds being half as large as inhibitory thresholds. The variability in threshold among afferents was directly related to neuronal gain and did not depend on spike count variance. The exact threshold values depended on both the time window used for spike count analysis and the filtering method used to calculate mean firing rate, although differences between regular and irregular afferent thresholds were independent of analysis parameters. The fact that minimum thresholds measured in macaque otolith afferents are of the same order of magnitude as human behavioral thresholds suggests that the vestibular periphery might determine the limit on our ability to detect or discriminate small differences in head movement, with little noise added during downstream processing

Maximizing decision rate in multisensory integration

Effective decision-making in an uncertain world requires making use of all available information, even if distributed across different sensory modalities, as well as trading off the speed of a decision with its accuracy. In tasks with a fixed stimulus presentation time, animal and human subjects have previously been shown to combine information from several modalities in a statistically optimal manner. Furthermore, for easily discriminable stimuli and under the assumption that reaction times result from a race-to-threshold mechanism, multimodal reaction times are typically faster than predicted from unimodal conditions when assuming independent (parallel) races for each modality. However, due to a lack of adequate ideal observer models, it has remained unclear whether subjects perform optimal cue combination when they are allowed to choose their response times freely.
Based on data collected from human subjects performing a visual/vestibular heading discrimination task, we show that the subjects exhibit worse discrimination performance in the multimodal condition than predicted by standard cue combination criteria, which relate multimodal discrimination performance to sensitivity in the unimodal conditions. Furthermore, multimodal reaction times are slower than those predicted by a parallel race model, opposite to what is commonly observed for easily discriminable stimuli.
Despite violating the standard criteria for optimal cue combination, we show that subjects still accumulate evidence optimally across time and cues, even when the strength of the evidence varies with time. Additionally, subjects adjust their decision bounds, controlling the trade-off between speed and accuracy of a decision, such that they feature correct decision rates close to the maximum achievable value

Representation of vestibular and visual cues to self-motion in ventral intraparietal cortex

Convergence of vestibular and visual motion information is important for self-motion perception. One cortical area that combines vestibular and optic flow signals is the ventral intraparietal area (VIP). We characterized unisensory and multisensory responses of macaque VIP neurons to translations and rotations in three dimensions. Approximately half of VIP cells show significant directional selectivity in response to optic flow, half show tuning to vestibular stimuli, and one-third show multisensory responses. Visual and vestibular direction preferences of multisensory VIP neurons could be congruent or opposite. When visual and vestibular stimuli were combined, VIP responses could be dominated by either input, unlike medial superior temporal area (MSTd) where optic flow tuning typically dominates or the visual posterior sylvian area (VPS) where vestibular tuning dominates. Optic flow selectivity in VIP was weaker than in MSTd but stronger than in VPS. In contrast, vestibular tuning for translation was strongest in VPS, intermediate in VIP, and weakest in MSTd. To characterize response dynamics, direction-time data were fit with a spatiotemporal model in which temporal responses were modeled as weighted sums of velocity, acceleration, and position components. Vestibular responses in VIP reflected balanced contributions of velocity and acceleration, whereas visual responses were dominated by velocity. Timing of vestibular responses in VIP was significantly faster than in MSTd, whereas timing of optic flow responses did not differ significantly among areas. These findings suggest that VIP may be proximal to MSTd in terms of vestibular processing but hierarchically similar to MSTd in terms of optic flow processing

A comparison of vestibular spatiotemporal tuning in macaque parietoinsular vestibular cortex, ventral intraparietal area, and medial superior temporal area

Vestibular responses have been reported in the parieto-insular vestibular cortex (PIVC), the ventral intraparietal area (VIP) and the dorsal medial superior temporal area (MSTd) of macaques. However, differences between areas remain largely unknown and it is not clear whether there is a hierarchy in cortical vestibular processing. We examine the spatiotemporal characteristics of macaque vestibular responses to translational motion stimuli using both empirical and model-based analyses. Temporal dynamics of direction selectivity were similar across areas, although there was a gradual shift in the time of peak directional tuning, with responses in MSTd typically being delayed by 100–150 ms relative to responses in PIVC (VIP was intermediate). Responses as a function of both stimulus direction and time were fit with a spatiotemporal model consisting of separable spatial and temporal response profiles. Temporal responses were characterized by a Gaussian function of velocity, a weighted sum of velocity and acceleration, or a weighted sum of velocity, acceleration, and position. Velocity and acceleration components contributed most to response dynamics, with a gradual shift from acceleration dominance in PIVC to velocity dominance in MSTd. The position component contributed little to temporal responses overall, but was substantially larger in MSTd than PIVC or VIP. The overall temporal delay in model fits also increased substantially from PIVC to VIP to MSTd. This gradual transformation of temporal responses suggests a hierarchy in cortical vestibular processing, with PIVC being most proximal to the vestibular periphery and MSTd being most distal

Convergence of vestibular and visual self-motion signals in an area of the posterior sylvian fissure

Convergence of visual motion information (optic flow) and vestibular signals is important for self-motion perception, and such convergence has been observed in the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas. In contrast, the parieto-insular vestibular cortex (PIVC), a cortical vestibular area in the sylvian fissure, is not responsive to optic flow. Here we explore optic flow and vestibular convergence in the visual posterior sylvian area (VPS) of macaque monkeys. This area is located at the posterior end of the sylvian fissure, is strongly interconnected with PIVC, and receives projections from MSTd. We found robust optic flow and vestibular tuning in more than one-third of VPS cells, with all motion directions being represented uniformly. However, visual and vestibular direction preferences for translation were mostly opposite, unlike in area MSTd where roughly equal proportions of neurons have visual/vestibular heading preferences that are congruent or opposite. Overall, optic flow responses in VPS were weaker than those in MSTd, whereas vestibular responses were stronger in VPS than in MSTd. When visual and vestibular stimuli were presented together, VPS responses were dominated by vestibular signals, in contrast to MSTd, where optic flow tuning typically dominates. These findings suggest that VPS is proximal to MSTd in terms of vestibular processing, but distal to MSTd in terms of optic flow processing. Given the preponderance of neurons with opposite visual/vestibular heading preferences in VPS, this area may not play a major role in multisensory heading perception

Multisensory calibration Is independent of cue reliability

Multisensory calibration is fundamental for proficient interaction within a changing environment. Initial studies suggested a visual-dominant mechanism. More recently, a cue-reliability based model, similar to optimal cue-integration, has been proposed. However, a more general, reliability-independent model of fixed-ratio adaptation (of which visual-dominance is a sub-case) has never been tested. Here, we studied behavior of both humans and monkeys performing a heading-discrimination task. Subjects were presented with either visual (optic-flow), vestibular (motion-platform) or combined (visual/vestibular) stimuli, and required to report whether self-motion was to the right/left of straight ahead. A systematic heading-discrepancy was introduced between the visual and vestibular cues, without external feedback. Cue-calibration was measured by the resulting sensory adaptation. Both visual and vestibular cues significantly adapted in the direction required to reduce cue-conflict. However, unlike multisensory cue-integration, cue-calibration was not reliability-based. Rather, a model of fixed-ratio adaptation best described the data, whereby vestibular adaptation was greater than visual adaptation, irrespective of relative cue-reliability. The average ratio of vestibular to visual adaptation was 1.75 and 2.30 for the human and monkey data, respectively. Furthermore, only through modeling fixed-ratio adaptation (using the ratio extracted from the data), were we were able to account for reliability-based cue-integration during the adaptation process. The finding that cue-calibration does not depend on cue-reliability is consistent with the notion that it follows an underlying estimate of cue-accuracy. Cue-accuracy is generally independent of cue-reliability and its estimate may change with a much slower time-constant. Thus, greater vestibular vs. visual (fixed-ratio) adaptation suggests lower vestibular vs. visual cue-accuracy

Relationship between complex and simple spike activity in macaque caudal vermis during three-dimensional vestibular stimulation

Lobules 10 and 9 in the caudal posterior vermis [also known as nodulus and uvula (NU)] are thought important for spatial orientation and balance. Here, we characterize complex spike (CS) and simple spike (SS) activity in response to three-dimensional vestibular stimulation. The strongest modulation was seen during translation (CS: 12.8 ± 1.5, SS: 287.0 ± 23.2 spikes/s/G, 0.5 Hz). Preferred directions tended to cluster along the cardinal axes (lateral, fore-aft, vertical) for CSs and along the semicircular canal axes for SSs. Most notably, the preferred directions for CS/SS pairs arising from the same Purkinje cells were rarely aligned. During 0.5 Hz pitch/roll tilt, only about a third of CSs had significant modulation. Thus, most CSs correlated best with inertial rather than net linear acceleration. By comparison, all SSs were selective for translation and ignored changes in spatial orientation relative to gravity. Like SSs, tilt modulation of CSs increased at lower frequencies. CSs and SSs had similar response dynamics, responding to linear velocity during translation and angular position during tilt. The most salient finding is that CSs did not always modulate out-of-phase with SSs. The CS/SS phase difference varied broadly among Purkinje cells, yet for each cell it was precisely matched for the otolith-driven and canal-driven components of the response. These findings illustrate a spatiotemporal mismatch between CS/SS pairs and provide the first comprehensive description of the macaque NU, an important step toward understanding how CSs and SSs interact during complex movements and spatial disorientation

Role of visual and non-visual cues in constructing a rotation-invariant representation of heading in parietal cortex

As we navigate through the world, eye and head movements add rotational velocity patterns to the retinal image. When such rotations accompany observer translation, the rotational velocity patterns must be discounted to accurately perceive heading. The conventional view holds that this computation requires efference copies of self-generated eye/head movements. Here we demonstrate that the brain implements an alternative solution in which retinal velocity patterns are themselves used to dissociate translations from rotations. These results reveal a novel role for visual cues in achieving a rotation-invariant representation of heading in the macaque ventral intraparietal area. Specifically, we show that the visual system utilizes both local motion parallax cues and global perspective distortions to estimate heading in the presence of rotations. These findings further suggest that the brain is capable of performing complex computations to infer eye movements and discount their sensory consequences based solely on visual cues. DOI: http://dx.doi.org/10.7554/eLife.04693.00

Vestibular heading discrimination and sensitivity to linear acceleration in head and world coordinates

Effective navigation and locomotion depend critically on an observer\u27s ability to judge direction of linear self-motion, i.e., heading. The vestibular cue to heading is the direction of inertial acceleration that accompanies transient linear movements. This cue is transduced by the otolith organs. The otoliths also respond to gravitational acceleration, so vestibular heading discrimination could depend on (1) the direction of movement in head coordinates (i.e., relative to the otoliths), (2) the direction of movement in world coordinates (i.e., relative to gravity), or (3) body orientation (i.e., the direction of gravity relative to the otoliths). To quantify these effects, we measured vestibular and visual discrimination of heading along azimuth and elevation dimensions with observers oriented both upright and side-down relative to gravity. We compared vestibular heading thresholds with corresponding measurements of sensitivity to linear motion along lateral and vertical axes of the head (coarse direction discrimination and amplitude discrimination). Neither heading nor coarse direction thresholds depended on movement direction in world coordinates, demonstrating that the nervous system compensates for gravity. Instead, they depended similarly on movement direction in head coordinates (better performance in the horizontal plane) and on body orientation (better performance in the upright orientation). Heading thresholds were correlated with, but significantly larger than, predictions based on sensitivity in the coarse discrimination task. Simulations of a neuron/anti-neuron pair with idealized cosine-tuning properties show that heading thresholds larger than those predicted from coarse direction discrimination could be accounted for by an amplitude-response nonlinearity in the neural representation of inertial motion