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

Perception of the Body in Space: Mechanisms

The principal topic is the perception of body orientation and motion in space and the extent to which these perceptual abstraction can be related directly to the knowledge of sensory mechanisms, particularly for the vestibular apparatus. Spatial orientation is firmly based on the underlying sensory mechanisms and their central integration. For some of the simplest situations, like rotation about a vertical axis in darkness, the dynamic response of the semicircular canals furnishes almost enough information to explain the sensations of turning and stopping. For more complex conditions involving multiple sensory systems and possible conflicts among their messages, a mechanistic response requires significant speculative assumptions. The models that exist for multisensory spatial orientation are still largely of the non-rational parameter variety. They are capable of predicting relationships among input motions and output perceptions of motion, but they involve computational functions that do not now and perhaps never will have their counterpart in central nervous system machinery. The challenge continues to be in the iterative process of testing models by experiment, correcting them where necessary, and testing them again

Purkinje Cells in Posterior Cerebellar Vermis Encode Motion in an Inertial Reference Frame

SummaryThe ability to orient and navigate through the terrestrial environment represents a computational challenge common to all vertebrates. It arises because motion sensors in the inner ear, the otolith organs, and the semicircular canals transduce self-motion in an egocentric reference frame. As a result, vestibular afferent information reaching the brain is inappropriate for coding our own motion and orientation relative to the outside world. Here we show that cerebellar cortical neuron activity in vermal lobules 9 and 10 reflects the critical computations of transforming head-centered vestibular afferent information into earth-referenced self-motion and spatial orientation signals. Unlike vestibular and deep cerebellar nuclei neurons, where a mixture of responses was observed, Purkinje cells represent a homogeneous population that encodes inertial motion. They carry the earth-horizontal component of a spatially transformed and temporally integrated rotation signal from the semicircular canals, which is critical for computing head attitude, thus isolating inertial linear accelerations during navigation

Research on integration of visual and motion cues for flight simulation and ride quality investigation

Vestibular perception and integration of several sensory inputs in simulation were studied. The relationship between tilt sensation induced by moving fields and those produced by actual body tilt is discussed. Linearvection studies were included and the application of the vestibular model for perception of orientation based on motion cues is presented. Other areas of examination includes visual cues in approach to landing, and a comparison of linear and nonlinear wash out filters using a model of the human vestibular system is given

Noise and vestibular perception of passive self-motion

Noise defined as random disturbances is ubiquitous in both the external environment and the nervous system. Depending on the context, noise can degrade or improve information processing and performance. In all cases, it contributes to neural systems dynamics. We review some effects of various sources of noise on the neural processing of self-motion signals at different stages of the vestibular pathways and the resulting perceptual responses. Hair cells in the inner ear reduce the impact of noise by means of mechanical and neural filtering. Hair cells synapse on regular and irregular afferents. Variability of discharge (noise) is low in regular afferents and high in irregular units. The high variability of irregular units provides information about the envelope of naturalistic head motion stimuli. A subset of neurons in the vestibular nuclei and thalamus are optimally tuned to noisy motion stimuli that reproduce the statistics of naturalistic head movements. In the thalamus, variability of neural discharge increases with increasing motion amplitude but saturates at high amplitudes, accounting for behavioral violation of Weber’s law. In general, the precision of individual vestibular neurons in encoding head motion is worse than the perceptual precision measured behaviorally. However, the global precision predicted by neural population codes matches the high behavioral precision. The latter is estimated by means of psychometric functions for detection or discrimination of whole-body displacements. Vestibular motion thresholds (inverse of precision) reflect the contribution of intrinsic and extrinsic noise to perception. Vestibular motion thresholds tend to deteriorate progressively after the age of 40 years, possibly due to oxidative stress resulting from high discharge rates and metabolic loads of vestibular afferents. In the elderly, vestibular thresholds correlate with postural stability: the higher the threshold, the greater is the postural imbalance and risk of falling. Experimental application of optimal levels of either galvanic noise or whole-body oscillations can ameliorate vestibular function with a mechanism reminiscent of stochastic resonance. Assessment of vestibular thresholds is diagnostic in several types of vestibulopathies, and vestibular stimulation might be useful in vestibular rehabilitation

Research on habituation to novel visual-vestibular environments with particular reference to space flight

Progress in the development of a cohesive theory of the underlying physiological mechanisms associated with spatial orientation in unusual environments is described. Results can be applied to providing means of preventing and/or minimizing the space motion sickness which has been observed during prolonged space missions. Three major areas were investigated: (1) the interaction of visual and vestibular cues in conflict in the human, (2) the plasticity of the vestibulo-ocular reflex in monkeys, and (3) end organ function in the ray with particular emphasis on the effect of ionic concentration

Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate

Galvanic vestibular stimulation (GVS) uses the external application of electrical current to selectively target the vestibular system in humans. Despite its recent popularity for the assessment/treatment of clinical conditions, exactly how this non-invasive tool activates the vestibular system remains an open question. Here we directly investigate single vestibular afferent responses to GVS applied to the mastoid processes of awake-behaving monkeys. Transmastoid GVS produces robust and parallel activation of both canal and otolith afferents. Notably, afferent activation increases with intrinsic neuronal variability resulting in constant GVS-evoked neuronal detection thresholds across all afferents. Additionally, afferent tuning differs for GVS versus natural self-motion stimulation. Using a stochastic model of repetitive activity in afferents, we largely explain the main features of GVS-evoked vestibular afferent dynamics. Taken together, our results reveal the neural substrate underlying transmastoid GVS-evoked perceptual, ocular and postural responses—information that is essential to advance GVS applicability for biomedical uses in humans

Connecting ears to eye muscles: Evolution of a 'simple' reflex arc

Developmental and evolutionary data from vertebrates are beginning to elucidate the origin of the sensorimotor pathway that links gravity and motion detection to image-stabilizing eye movements--the vestibulo-ocular reflex (VOR). Conserved transcription factors coordinate the development of the vertebrate ear into three functional sensory compartments (graviception/translational linear acceleration, angular acceleration and sound perception). These sensory components connect to specific populations of vestibular and auditory projection neurons in the dorsal hindbrain through undetermined molecular mechanisms. In contrast, a molecular basis for the patterning of the vestibular projection neurons is beginning to emerge. These are organized through the actions of rostrocaudally and dorsoventrally restricted transcription factors into a 'hodological mosaic' within which coherent and largely segregated subgroups are specified to project to different targets in the spinal cord and brain stem. A specific set of these regionally diverse vestibular projection neurons functions as the central element that transforms vestibular sensory signals generated by active and passive head and body movements into motor output through the extraocular muscles. The large dynamic range of motion-related sensory signals requires an organization of VOR pathways as parallel, frequency-tuned, hierarchical connections from the sensory periphery to the motor output. We suggest that eyes, ears and functional connections subserving the VOR are vertebrate novelties that evolved into a functionally coherent motor control system in an almost stereotypic organization across vertebrate taxa

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