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Quantifying the performance limits of human saccadic targeting during visual search

In previous studies of saccadic targeting, the issue how visually guided saccades to unambiguous targets are programmed and executed has been examined. These studies have found different degrees of guidance for saccades depending on the task and task difficulty. In this study, we use ideal-observer analysis to estimate the visual information used for the first saccade during a search for a target disk in noise. We quantitatively compare the performance of the first saccadic decision to that of the ideal observer (ie absolute efficiency of the first saccade) and to that of the associated final perceptual decision at the end of the search (ie relative efficiency of the first saccade). Our results show, first, that at all levels of salience tested, the first saccade is based on visual information from the stimulus display, and its highest absolute efficiency is approximately 20%. Second, the efficiency of the first saccade is lower than that of the final perceptual decision after active search (with eye movements) and has a minimum relative efficiency of 19% at the lowest level of saliency investigated. Third, we found that requiring observers to maintain central fixation (no saccades allowed) decreased the absolute efficiency of their perceptual decision by up to a factor of two, but that the magnitude of this effect depended on target salience. Our results demonstrate that ideal-observer analysis can be extended to measure the visual information mediating saccadic target-selection decisions during visual search, which enables direct comparison of saccadic and perceptual efficiencies.

Non-NASA Center

Shared motion signals for human perceptual decisions and oculomotor actions

A fundamental question in primate neurobiology is to understand to what extent motor behaviors are driven by shared neural signals that also support conscious perception or by independent subconscious neural signals dedicated to motor control. Although it has clearly been established that cortical areas involved in processing visual motion support both perception and smooth pursuit eye movements, it remains unknown whether the same or different sets of neurons within these structures perform these two functions. Examination of the trial-by-trial variation in human perceptual and pursuit responses during a simultaneous psychophysical and oculomotor task reveals that the direction signals for pursuit and perception are not only similar on average but also co-vary on a trial-by-trial basis, even when performance is at or near chance and the decisions are determined largely by neural noise. We conclude that the neural signal encoding the direction of target motion that drives steady-state pursuit and supports concurrent perceptual judgments emanates from a shared ensemble of cortical neurons.

Visual Cortex/physiology

Attentional sensitivity and asymmetries of vertical saccade generation in monkey

The first goal of this study was to systematically document asymmetries in vertical saccade generation. We found that visually guided upward saccades have not only shorter latencies, but higher peak velocities, shorter durations and smaller errors. The second goal was to identify possible mechanisms underlying the asymmetry in vertical saccade latencies. Based on a recent model of saccade generation, three stages of saccade generation were investigated using specific behavioral paradigms: attention shift to a visual target (CUED paradigm), initiation of saccade generation (GAP paradigm) and release of the motor command to execute the saccade (DELAY paradigm). Our results suggest that initiation of a saccade (or "ocular disengagement") and its motor release contribute little to the asymmetry in vertical saccade latency. However, analysis of saccades made in the CUED paradigm indicated that it took less time to shift attention to a target in the upper visual field than to a target in the lower visual field. These data suggest that higher attentional sensitivity to targets in the upper visual field may contribute to shorter latencies of upward saccades.

NASA Discipline Neuroscience

Spatial scale of motion segmentation from speed cues

For the accurate perception of multiple, potentially overlapping, surfaces or objects, the visual system must distinguish different local motion vectors and selectively integrate similar motion vectors over space to segment the retinal image properly. We recently showed that large differences in speed are required to yield a percept of motion transparency. In the present study, to investigate the spatial scale of motion segmentation from speed cues alone, we measured the speed-segmentation threshold (the minimum speed difference required for 75% performance accuracy) for 'corrugated' random-dot patterns, i.e. patterns in which dots with two different speeds were alternately placed in adjacent bars of variable width. In a first experiment, we found that, at large bar widths, a smaller speed difference was required to segment and perceive the corrugated pattern of moving dots, while at small bar-widths, a larger speed difference was required to segment the two speeds and perceive two transparent surfaces of moving dots. Both the perceptual and segmentation performance transitions occurred at a bar width of around 0.4 degrees. In a second experiment, speed-segmentation thresholds were found to increase sharply when dots with different speeds were paired within a local pooling area. The critical pairing distance was about 0.2 degrees in the fovea and increased linearly with stimulus eccentricity. However, across the range of eccentricities tested (up to 15 degrees ), the critical pairing distance did not change much and remained close to the receptive field size of neurons within the primate primary visual cortex. In a third experiment, increasing dot density changed the relationship between speed-segmentation thresholds and bar width. Thresholds decreased for large bar widths, but increased for small bar widths. All of these results are well fit by a simple stochastic model, which estimates the probabilities of having identical or different motion vectors within a local pooling area whose size is the same as that of primate V1 neurons. Altogether, these results demonstrate that speed-based segmentation can function well, even at small spatial scales (i.e. high-spatial frequencies of spatial corrugation) and thereby emphasizes the critical role of a local pooling process early in the cortical motion-processing pathway.

NASA Discipline Neuroscience

Exercise increases blood flow to locomotor, vestibular, cardiorespiratory and visual regions of the brain in miniature swine

1. The purpose of these experiments was to use radiolabelled microspheres to measure blood flow distribution within the brain, and in particular to areas associated with motor function, maintenance of equilibrium, cardiorespiratory control, vision, hearing and smell, at rest and during exercise in miniature swine. Exercise consisted of steady-state treadmill running at intensities eliciting 70 and 100 % maximal oxygen consumption (V(O(2),max)). 2. Mean arterial pressure was elevated by 17 and 26 % above that at rest during exercise at 70 and 100 % V(O(2),max), respectively. 3. Mean brain blood flow increased 24 and 25 % at 70 and 100 % V(O(2),max), respectively. Blood flow was not locally elevated to cortical regions associated with motor and somatosensory functions during exercise, but was increased to several subcortical areas that are involved in the control of locomotion. 4. Exercise elevated perfusion and diminished vascular resistance in several regions of the brain related to the maintenance of equilibrium (vestibular nuclear area, cerebellar ventral vermis and floccular lobe), cardiorespiratory control (medulla and pons), and vision (dorsal occipital cortex, superior colliculi and lateral geniculate body). Conversely, blood flow to regions related to hearing (cochlear nuclei, inferior colliculi and temporal cortex) and smell (olfactory bulbs and rhinencephalon) were unaltered by exercise and associated with increases in vascular resistance. 5. The data indicate that blood flow increases as a function of exercise intensity to several areas of the brain associated with integrating sensory input and motor output (anterior and dorsal cerebellar vermis) and the maintenance of equilibrium (vestibular nuclei). Additionally, there was an intensity-dependent decrease of vascular resistance in the dorsal cerebellar vermis.

Non-NASA Center

Stimulus-response incompatibility activates cortex proximate to three eye fields

We used functional magnetic resonance imaging (fMRI) to investigate cortical activation during the performance of three oculomotor tasks that impose increasing levels of cognitive demand. (1) In a visually guided saccade (VGS) task, subjects made saccades to flashed targets. (2) In a compatible task, subjects made leftward and rightward saccades in response to foveal presentation of the uppercase words "LEFT" or "RIGHT." (3) In a mixed task, subjects made rightward saccades in response to the lowercase word "left" and leftward saccades in response to the lowercase word "right" on incompatible trials (60%). The remaining 40% of trials required compatible responses to uppercase words. The VGS and compatible tasks, when compared to fixation, activated the three cortical eye fields: the supplementary eye field (SEF), the frontal eye field (FEF), and the parietal eye field (PEF). The mixed task, when compared to the compatible task, activated three additional cortical regions proximate to the three eye fields: (1) rostral to the SEF in medial frontal cortex; (2) rostral to the FEF in dorsolateral prefrontal cortex (DLPFC); (3) rostral and lateral to the PEF in posterior parietal cortex. These areas may contribute to the suppression of prepotent responses and in holding novel visuomotor associations in working memory. Copyright 2001 Academic Press.

NASA Discipline Neuroscience

Visual motion integration for perception and pursuit

To examine the relationship between visual motion processing for perception and pursuit, we measured the pursuit eye-movement and perceptual responses to the same complex-motion stimuli. We show that humans can both perceive and pursue the motion of line-figure objects, even when partial occlusion makes the resulting image motion vastly different from the underlying object motion. Our results show that both perception and pursuit can perform largely accurate motion integration, i.e. the selective combination of local motion signals across the visual field to derive global object motion. Furthermore, because we manipulated perceived motion while keeping image motion identical, the observed parallel changes in perception and pursuit show that the motion signals driving steady-state pursuit and perception are linked. These findings disprove current pursuit models whose control strategy is to minimize retinal image motion, and suggest a new framework for the interplay between visual cortex and cerebellum in visuomotor control.

NASA Center ARC

Formation of compact myelin is required for maturation of the axonal cytoskeleton

Although traditional roles ascribed to myelinating glial cells are structural and supportive, the importance of compact myelin for proper functioning of the nervous system can be inferred from mutations in myelin proteins and neuropathologies associated with loss of myelin. Myelinating Schwann cells are known to affect local properties of peripheral axons (de Waegh et al., 1992), but little is known about effects of oligodendrocytes on CNS axons. The shiverer mutant mouse has a deletion in the myelin basic protein gene that eliminates compact myelin in the CNS. In shiverer mice, both local axonal features like phosphorylation of cytoskeletal proteins and neuronal perikaryon functions like cytoskeletal gene expression are altered. This leads to changes in the organization and composition of the axonal cytoskeleton in shiverer unmyelinated axons relative to age-matched wild-type myelinated fibers, although connectivity and patterns of neuronal activity are comparable. Remarkably, transgenic shiverer mice with thin myelin sheaths display an intermediate phenotype indicating that CNS neurons are sensitive to myelin sheath thickness. These results indicate that formation of a normal compact myelin sheath is required for normal maturation of the neuronal cytoskeleton in large CNS neurons.

NASA Discipline Neuroscience

Efferent projections of the ectostriatum in the pigeon (Columba livia)

The ectostriatum is a major visual component of the avian telencephalon. The core region of the ectostriatum (Ec) receives visual input from the optic tectum through thalamic nuclei. In the present study, the efferent projections of the ectostriatum were investigated by using the anterograde tracers Phaseolus vulgaris leucoagglutinin and biotinylated dextran amine. Projection patterns resulting from these tracers were confirmed by the retrograde tracer cholera toxin subunit B. When anterograde tracers were injected in Ec, primary projections were seen traveling dorsolaterally to the belt region of the ectostriatum (Ep) and the neostriatal area immediately surrounding Ep (Ep2). Neurons in Ep sent projections primarily to the overlying Ep2. The efferents of Ep2 traveled dorsolaterally to terminate in three telencephalic regions, from anterior to posterior: (1) neostriatum frontale, pars lateralis (NFL), (2) area temporo-parieto-occipitalis (TPO), and (3) neostriatum intermedium, pars lateralis (NIL). A part of the archistriatum intermedium and the lateral part of the neostriatum caudale also received somewhat minor projections. In addition, some neurons in Ec were also the source of direct, but minor, projections to the NFL, TPO, NIL, and archistriatum intermedium. The topographical relationship among the primary (Ec), secondary (Ep and Ep2), and tertiary (NFL, TPO, NIL) areas indicate that the neural populations for visual processing are organized along the rostral-caudal axis. Thus, the anterior Ec sent efferents to the anterior Ep, which in turn sent projections to anterior Ep2. Neurons in the anterior Ep2 sent projections to NFL and the anterior TPO. Similarly, the intermediate and posterior Ec sent projections to corresponding parts of Ep, whose efferents projected to intermediate and posterior Ep2, respectively. The intermediate Ep2 gave rise to major projections to TPO, whereas posterior Ep2 neurons sent efferents primarily to NIL. The organization of this neural circuit is compared with those of other sensory circuits in the avian telencephalon, as well as the laminar arrangement of the mammalian isocortex.

Non-NASA Center

The effect of optokinetic stimulation on daytime sleepiness

This study examined the effect of optokinetic stimulation on objective sleepiness, as measured by the Multiple Sleep Latency Test (MSLT). The Nightcap, a portable sleep monitor, was used in a novel way to perform MSLTs, as well as record sleep in the home. Subjects wore the Nightcap for seven consecutive nights. On days 3 and 5 of the protocol, subjects came into the lab for an MSLT. On the experimental day, subjects underwent 10 minutes optokinetic stimulation (OKS), resulting in moderate motion sickness prior to each MSLT trial. Although subjects in the OKS condition reported significantly more drowsiness than controls, this did not result in significantly reduced sleep latencies.

NASA Discipline Neuroscience

Expansion of direction space around the cardinal axes revealed by smooth pursuit eye movements

It is well established that perceptual direction discrimination shows an oblique effect; thresholds are higher for motion along diagonal directions than for motion along cardinal directions. Here, we compare simultaneous direction judgments and pursuit responses for the same motion stimuli and find that both pursuit and perceptual thresholds show similar anisotropies. The pursuit oblique effect is robust under a wide range of experimental manipulations, being largely resistant to changes in trajectory (radial versus tangential motion), speed (10 versus 25 deg/s), directional uncertainty (blocked versus randomly interleaved), and cognitive state (tracking alone versus concurrent tracking and perceptual tasks). Our data show that the pursuit oblique effect is caused by an effective expansion of direction space surrounding the cardinal directions and the requisite compression of space for other directions. This expansion suggests that the directions around the cardinal directions are in some way overrepresented in the visual cortical pathways that drive both smooth pursuit and perception.

Visual Pathways/physiology

Stimulus information contaminates summation tests of independent neural representations of features

Many models of visual processing assume that visual information is analyzed into separable and independent neural codes, or features. A common psychophysical test of independent features is known as a summation study, which measures performance in a detection, discrimination, or visual search task as the number of proposed features increases. Improvement in human performance with increasing number of available features is typically attributed to the summation, or combination, of information across independent neural coding of the features. In many instances, however, increasing the number of available features also increases the stimulus information in the task, as assessed by an optimal observer that does not include the independent neural codes. In a visual search task with spatial frequency and orientation as the component features, a particular set of stimuli were chosen so that all searches had equivalent stimulus information, regardless of the number of features. In this case, human performance did not improve with increasing number of features, implying that the improvement observed with additional features may be due to stimulus information and not the combination across independent features.

NASA Discipline Space Human Factors

Yaw sensory rearrangement alters pitch vestibulo-ocular reflex responses

Ten male subjects underwent two types of adaptation paradigm designed either to enhance or to attenuate the gain of the canal-ocular reflex (COR), before undergoing otolith-ocular reflex (OOR) testing with constant velocity, earth horizontal axis and pitch rotation. The adaptation paradigm paired a 0.2 Hz sinusoidal rotation about an earth vertical axis with a 0.2 Hz optokinetic stimulus that was deliberately mismatched in peak velocity or phase and was designed to produce short-term changes in the COR. Preadaptation and postadaptation OOR tests occurred at a constant velocity of 60 degrees/sec in the dark and produced a modulation component of the slow phase velocity with a frequency of 0.16 Hz due to otolithic stimulation by the sinusoidally changing gravity vector. Of the seven subjects who showed enhancement of the COR gain, six also showed enhancement of the OOR modulation component. Of the seven subjects who showed attenuation of the COR gain, five also showed attenuation of the OOR modulation component. The probability that these two cross-axis adaptation effects would occur by chance is less than 0.02. This suggests that visual-vestibular conditioning of the yaw axis COR also induced changes in the pitch axis OOR. We thus postulate that the central nervous system pathways that process horizontal canal yaw stimuli have elements in common with those processing otolithic stimuli about the pitch axis.

NASA Discipline Neuroscience

A common network of functional areas for attention and eye movements

Functional magnetic resonance imaging (fMRI) and surface-based representations of brain activity were used to compare the functional anatomy of two tasks, one involving covert shifts of attention to peripheral visual stimuli, the other involving both attentional and saccadic shifts to the same stimuli. Overlapping regional networks in parietal, frontal, and temporal lobes were active in both tasks. This anatomical overlap is consistent with the hypothesis that attentional and oculomotor processes are tightly integrated at the neural level.

Non-NASA Center

Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20 degrees /s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non-eye-movement (n = 52) and eye-movement-related (n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 +/- 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement-related units tended to have rotational responses that were correlated with head velocity. On the other hand, non-eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.

Non-NASA Center

Differential central projections of vestibular afferents in pigeons

The question of whether a differential distribution of vestibular afferent information to central nuclear neurons is present in pigeons was studied using neural tracer compounds. Discrete tracing of afferent fibers innervating the individual semicircular canal and otolith organs was produced by sectioning individual branches of the vestibular nerve that innervate the different receptor organs and applying crystals of horseradish peroxidase, or a horseradish peroxidase/cholera toxin mixture, or a biocytin compound for neuronal uptake and transport. Afferent fibers and their terminal distributions within the brainstem and cerebellum were visualized subsequently. Discrete areas in the pigeon central nervous system that receive primary vestibular input include the superior, dorsal lateral, ventral lateral, medial, descending, and tangential vestibular nuclei; the A and B groups; the intermediate, medial, and lateral cerebellar nuclei; and the nodulus, the uvula, and the paraflocculus. Generally, the vertical canal afferents projected heavily to medial regions in the superior and descending vestibular nuclei as well as the A group. Vertical canal projections to the medial and lateral vestibular nuclei were observed but were less prominent. Horizontal canal projections to the superior and descending vestibular nuclei were much more centrally located than those of the vertical canals. A more substantial projection to the medial and lateral vestibular nuclei was seen with horizontal canal afferents compared to vertical canal fibers. Afferents innervating the utricle and saccule terminated generally in the lateral regions of all vestibular nuclei in areas that were separate from the projections of the semicircular canals. In addition, utricular fibers projected to regions in the vestibular nuclei that overlapped with the horizontal semicircular canal terminal fields, whereas saccular afferents projected to regions that received vertical canal fiber terminations. Lagenar afferents projected throughout the cochlear nuclei, to the dorsolateral regions of the cerebellar nuclei, and to lateral regions of the superior, lateral, medial, and descending vestibular nuclei.

NASA Discipline Neuroscience