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The impact of aging on curiosity as measured by exploratory eye movements.

OBJECTIVE: To investigate changes in novelty-seeking behavior (curiosity) associated with normal aging. BACKGROUND: Recently, we demonstrated that patients with a diagnosis of probable Alzheimer's disease display diminished novelty-seeking behavior as measured by exploratory eye movements. Nondemented, elderly individuals are often depicted in clinical descriptions as exhibiting diminished curiosity and increased disengagement from their surroundings. However, this behavior has not been systematically investigated as a function of normal aging. SETTING: University hospital center studying aging and dementia. SUBJECTS: Fourteen active, healthy elderly subjects (mean age, 72 years) and 16 middle-aged subjects (mean age, 42 years) matched for education and estimated IQ. MEASURES: Exploratory eye movements were recorded in response to visual stimuli that varied in novelty, complexity, and incongruity. RESULTS: Both older and middle-aged subjects (1) spent significantly more time exploring the more irregular or incongruous of two simultaneously presented stimuli, (2) spent increasingly less time looking at a repeating visual stimulus paired with a stimulus that changed with each trial, and (3) exhibited the same degree of overall exploration of a visual scene and devoted an approximately equal amount of attention to an unexpected element within it. As a group, older subjects spent slightly less time than middle-aged subjects examining incongruous stimuli. However, 71% (10/14) of older subjects performed within 1 SD of the mean of middle-aged subjects and 21% (3/14) performed as well as the top 50% (8/16) of middle-aged controls. CONCLUSIONS: The drive for curiosity, as measured by exploratory eye movements, can be well preserved in older individuals. Further research is needed to determine if the integrity of this drive can serve as a marker of "successful aging" and to identify which physiological and psychological factors influence its preservation through the life cycle.

Adult↗

Cross-axis adaptation of torsional components in the yaw-axis vestibulo-ocular reflex.

The three pairs of semicircular canals within the labyrinth are not perfectly aligned with the pulling directions of the six extraocular muscles. Therefore, for a given head movement, the vestibulo-ocular reflex (VOR) depends upon central neural mechanisms that couple the canals to the muscles with the appropriate functional gains in order to generate a response that rotates the eye the correct amount and around the correct axis. A consequence of these neural connections is a cross-axis adaptive capability, which can be stimulated experimentally when head rotation is around one axis and visual motion about another. From this visual-vestibular conflict the brain infers that the slow-phase eye movement is rotating around the wrong axis. We explored the capability of human cross-axis adaptation, using a short-term training paradigm, to determine if torsional eye movements could be elicited by yaw (horizontal) head rotation (where torsion is normally inappropriate). We applied yaw sinusoidal head rotation (+/-10 degrees, 0.33 Hz) and measured eye movement responses in the dark, and before and after adaptation. The adaptation paradigm lasted 45-60 min, and consisted of the identical head motion, coupled with a moving visual scene that required one of several types of eye movements: (1) torsion alone (-Roll); (2) horizontal/torsional, head right/CW torsion (Yaw-Roll); (3) horizontal/torsional, head right/CCW torsion (Yaw+Roll); (4) horizontal, vertical, torsional combined (Yaw+Pitch-Roll); and (5) horizontal and vertical together (Yaw+Pitch). The largest and most significant changes in torsional amplitude occurred in the Yaw-Roll and Yaw+Roll conditions. We conclude that short-term, cross-axis adaptation of torsion is possible but constrained by the complexity of the adaptation task: smaller torsional components are produced if more than one cross-coupling component is required. In contrast, vertical cross-axis components can be easily trained to occur with yaw head movements.

Adaptation, Physiological↗

The selective disruption of spatial working memory by eye movements.

In the late 1970s/early 1980s, Baddeley and colleagues conducted a series of experiments investigating the role of eye movements in visual working memory. Although only described briefly in a book, these studies have influenced a remarkable number of empirical and theoretical developments in fields ranging from experimental psychology to human neuropsychology to nonhuman primate electrophysiology. This paper presents, in full detail, three critical studies from this series, together with a recently performed study that includes a level of eye movement measurement and control that was not available for the older studies. Together, the results demonstrate several facts about the sensitivity of visuospatial working memory to eye movements. First, it is eye movement control, not movement per se, that produces the disruptive effects. Second, these effects are limited to working memory for locations and do not generalize to visual working memory for shapes. Third, they can be isolated to the storage/maintenance components of working memory (e.g., to the delay period of the delayed-recognition task). These facts have important implications for models of visual working memory.

Adolescent↗

Automatic generation of a retinal sensitivity map using infra-red fundus television images.

We have already developed an eye movement analyzing system using an infra-red television fundus camera. Although the quality of the fundus TV images is not good, the system can measure eye movement with an accuracy order of 0.1 degree. We try to apply this system to compensating for eye movements in producing a retinal sensitivity map. A target with variable brightness is presented to various positions on the retina of a subject through a CRT assembled in the infra-red TV fundus camera. The subject is supposed to respond if he can perceive the target. The TV image of the eye fundus, together with the overlaid target and response sign, is recorded on a U-matic (3/4 in) VTR. The image of the video tape is then analyzed by a computer. We have obtained retinal sensitivity maps which show good agreement with the results obtained using the Goldmann perimeter.

Equipment Design↗

A general numerical method evaluating three-dimensional eye rotations by scanning laser ophthalmoscopy.

A general computational method is described to specify completely the rotational state of the eye in three dimensions by scanning laser ophthalmoscopy (SLO). The method uses the simplex algorithm to fit the eye's rotational parameters to data given by n individually selected ocular fundus landmarks before and after the eye rotation. The rotational parameters are expressed as the rotation vector and three spherical Euler angles. The method, which was implemented in the C programming language, can be applied for various eye movement measurements in clinical and laboratory environments, including SLO.

Algorithms↗

Comparison of vestibular autorotation and caloric testing.

The two most common stimuli of the vestibular system for diagnostic purposes are caloric and rotational head movements. Caloric stimulation, by delivering thermal energy to the lateral semicircular canal, is a well-studied method of vestibular testing, and its clinical usefulness has been established. Vestibular autorotation testing uses high-frequency (2 to 6 Hz), active head movements to stimulate the horizontal and vertical vestibulo-ocular reflex to produce measurable eye movements that can be used to calculate gain and phase. We compared the alternate bilateral bithermal caloric results with the vestibular autorotation test results obtained from 39 patients with peripheral vestibular disorders and from 10 patients with acoustic neuroma. In the peripheral disorder group, only 2 of 14 patients with equal caloric response (< 20% reduced vestibular response) had a normal vestibular autorotation test result. No patients with a reduced vestibular response greater than 21% had a normal vestibular autorotation test result. In the acoustic neuroma group, four patients had a normal reduced vestibular response, but all patients had an abnormal vestibular autorotation test result. We conclude that testing both the horizontal and vertical vestibulo-ocular reflexes in their physiologic frequency range with the vestibular autorotation test provides additional information that could be missed by conventional caloric testing. Therefore high-frequency rotational testing is a valuable addition to the vestibular test battery.

Adult↗

Ocular oscillations induced by shifts of the direction and depth of visual fixation.

Shifts of the point of fixation between two targets aligned on one eye that are located near and far (Müller paradigm) stimulates a combined saccadic-vergence movement. In normal subjects, this test paradigm often induces saccadic oscillations of about 0.3 degrees at 20 to 30 Hz. We measured eye movements using the magnetic search coil technique in 2 patients recovering from viral opsoclonus-myoclonus syndrome, comparing saccadic-vergence responses to the Müller paradigm with conjugate saccades between distant targets. Both patients exhibited intermittent conjugate ocular oscillations of about 4 to 5 degrees amplitude at about 10 Hz. Combined saccadic-vergence movements induced these oscillations twice as often as did conjugate saccades. One patient also exhibited disjunctive ocular oscillations at 10 Hz while sustaining fixation on the near target. The Müller paradigm provides a useful clinical and experimental technique for inducing saccadic oscillations. The probable mechanism is that pontine omnipause neurons, which normally gate saccades, are inhibited during the sustained vergence movement that follows the saccadic component of the response to the Müller paradigm.

Adult↗

Eye movement detector calibration device.

Presented is a device developed for specifically calibrating and validating the operation of Eye Movement Detectors or Monitors. The Calibrator centers on two one inch diameter HPDE spheres representing the eyes. A Laser Module is embedded in the rear of each sphere emitting a beam against a target divided in equal measurement intervals mounted as part of the device. The device moves the "eyes" about its center axes enabling the user to validate any vertical, horizontal, or X-Y combination eye position in a plus or minus fifteen degree range. Although hand controlled, the Calibrator can be motorized with stepper motors or other desired drivers. Anatomically correct sized pupils are imbedded in the front of each "eye," thereby acting as the target for whichever system is under test by the very portable Calibrator. Currently, a simple battery controlled circuit controls the laser modules and other electric requirements with accommodation for additional circuit components if required in the future. Specifically designed for validating the operation of an IR Reflective Differencing Saccadic Eye Movement Measurement System, the Calibrator can also be used with little or no alteration for validation of camera systems and other types of devices.

Calibration↗

Eye-movement recordings in the evaluation of ophthalmologic and neurologic disorders.

This review focuses on the use of quantitative eye-movement recordings in the diagnosis of ophthalmologic and neurologic disorders and in the investigation of the pathophysiologic mechanisms of and possible treatments for these disorders. Recently developed methods for measuring eye movements about all three axes of rotation (horizontal, vertical, and torsion) are emphasized. These techniques are providing important insights into the basic physiology of eye-movement control and into the mechanisms of ocular motor disturbances in which torsion plays a significant role.

Diagnosis, Differential↗

Diminished curiosity in patients with probable Alzheimer's disease as measured by exploratory eye movements.

Clinical accounts of Alzheimer's disease (AD) suggest that some patients exhibit markedly diminished curiosity and initiative early in the course of their illness. Such behavioral changes are extremely difficult to measure experimentally. We studied one aspect of curiosity by measuring exploratory eye movements in response to provocative visual stimuli in 12 patients with probable AD and 10 matched controls. Subjects viewed slides, each of which contained an incongruous or irregular figure paired with a congruous or regular one. Unlike controls, who spent significantly more time viewing the incongruous stimuli, AD patients distributed their viewing time equally and spent significantly less time than controls looking at the novel stimuli. Additionally, when presented with picture slides containing an unexpected element, AD patients exhibited diminished visual exploration overall and decreased attention to the incongruous part. Further analyses suggest that the results cannot be adequately explained by a general decline in cognition or by problems with ocular motility or directing visual attention. We conclude that AD patients exhibit diminished curiosity which can be measured by the study of exploratory eye movements.

Aged↗

A proposed neural network for the integrator of the oculomotor system.

Single-unit recordings, stimulation studies, and eye movement measurements all indicate that the firing patterns of many oculomotor neurons in the brain stem encode eye-velocity commands in premotor circuits while the firing patterns of extraocular motoneurons contain both eye-velocity and eye-position components. It is necessary to propose that the eye-position component is generated from the eye-velocity signal by a leaky hold element or temporal integrator. Prior models of this integrator suffer from two important problems. Since cells appear to have a steady, background signal when eye position and velocity are zero, how does the integrator avoid integrating this background rate? Most models employ some form of lumped, positive feedback the gain of which must be kept within totally unreasonable limits for proper operation. We propose a lateral inhibitory network of homogeneous neurons as a model for the neural integrator that solves both problems. Parameter sensitivity studies and lesion simulations are presented to demonstrate robustness of the model with respect to both the choice of parameter values and the consequences of pathological changes in a portion of the neural integrator pool.

Animals↗

Detection of differential viewing patterns to erotic and non-erotic stimuli using eye-tracking methodology.

As a first step in the investigation of the role of visual attention in the processing of erotic stimuli, eye-tracking methodology was employed to measure eye movements during erotic scene presentation. Because eye-tracking is a novel methodology in sexuality research, we attempted to determine whether the eye-tracker could detect differences (should they exist) in visual attention to erotic and non-erotic scenes. A total of 20 men and 20 women were presented with a series of erotic and non-erotic images and tracked their eye movements during image presentation. Comparisons between erotic and non-erotic image groups showed significant differences on two of three dependent measures of visual attention (number of fixations and total time) in both men and women. As hypothesized, there was a significant Stimulus x Scene Region interaction, indicating that participants visually attended to the body more in the erotic stimuli than in the non-erotic stimuli, as evidenced by a greater number of fixations and longer total time devoted to that region. These findings provide support for the application of eye-tracking methodology as a measure of visual attentional capture in sexuality research. Future applications of this methodology to expand our knowledge of the role of cognition in sexuality are suggested.

Adult↗

Eye movements during reading: some current controversies.

For many researchers, eye-movement measures have become instrumental in revealing the moment-to-moment activity of the mind during reading. In general, there has been a great deal of consistency across studies within the eye-movement literature, and researchers have discovered and examined many variables involved in the reading process that affect the nature of readers' eye movements. Despite remarkable progress, however, there are still a number of issues to be resolved. In this article, we discuss three controversial issues: (1) the extent to which eye-movement behavior is affected by low-level oculomotor factors versus higher-level cognitive processes; (2) how much information is extracted from the right of fixation; and (3) whether readers process information from more than one word at a time.

Journal Article↗

Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement.

Single units were recorded from the vestibular nuclei of unanesthetized monkeys that were rotated in the horizontal plane while simultaneously pressing individual buttons in a controlled array which turned with hem. Using this behavioral paradigm, it was possible to 1) determine the relationship of unit discharge to eye movements measured by the DC-coupled electrooculogram and calibrated by the button-press task, and 2) determine the relationship of unit discharge to horizontal acceleration, either with or without the compensatory eye movements evoked by vestibular stimulation. Based on their responses during vestibular stimulation and/or eye movements, neurons in the vestibular nuclei (77% of our sample was in the medial nucleus) could be divided into four groups...

Acceleration↗

Identifying psychophysiological risk for psychopathology: examples from substance abuse and schizophrenia research.

A problem confronting the search for psychopathology-related genes concerns the difficulty identifying gene carriers. Psychiatric diagnosis provides imperfect identification of affected individuals, and unaffected gene carriers go undetected. Psychophysiological measures may assist molecular genetic investigations by indicating genetic susceptibility for psychopathology, thus increasing the probability of identifying affected and unaffected gene carriers. Research strategies based on these premises are applied to the study of psychoactive substance use disorders and schizophrenia. Data are presented illustrating (1) that individual differences in inhibitory control involving autonomic and antisaccade eye movement measures and the P3 component of the event-related potential may be sensitive to susceptibility for substance use disorders, and (2) that eye tracking variables may identify genetic risk for schizophrenia.

Alcoholism↗

Simultaneous opposing adaptive changes in cat vestibulo-ocular reflex direction for two body orientations.

The specificity of adaptation of vestibulo-ocular reflex direction was examined by exposing cats to combined pitch vestibular rotation and horizontal optokinetic motion at 0.25 Hz, while alternating body position between lying on the left side and lying on the right. The direction of optokinetic motion relative to head motion was reversed when the cat's body posture was changed so that, for example, if head upward rotation was coupled to leftward visual world motion when the cat was lying on its left side, then head upward rotation was coupled to rightward visual world motion when the cat was on its right side. Body position and optokinetic motion direction were changed every 10 min for a total of 2 h of adaptation on each side. Horizontal and vertical electrooculographic recordings were made during pitch rotations in darkness before and after adaptation. Saccades were removed from the records and vestibulo-ocular reflex gain was measured in the direction of optokinetic motion. In every case, the adaptation procedure produced a directional change in the vestibulo-ocular reflex specific to the posture during measurement and appropriate to reduce the retinal image motion caused by the combined vestibular and optokinetic stimuli. That is, adaptive horizontal eye movements measured on the two sides were in opposite directions for the same direction of head motion. This specificity suggests that adaptation of vestibulo-ocular reflex direction involves specific neural pathways that are controlled by body orientation signals which most likely arise from the otolith organs.

Adaptation, Physiological↗

Neural response to emotional salience in schizophrenia.

Neuroimaging probes of brain regions implicated in emotion represent an important research strategy for understanding emotional dysfunction in schizophrenia. Anterior limbic structures, such as the ventral striatum and the amygdala, have been implicated in the pathophysiology of schizophrenia and the generation of emotional responses, although few studies to date have used emotion probes to target these areas in schizophrenia. With this goal in mind, emotionally salient visual images were used in a simple, nondemanding task. In all, 13 medicated, schizophrenic patients, five unmedicated patients, and 10 healthy volunteers viewed complex visual pictures and a nonsalient, blank screen while regional cerebral blood flow was measured with the [O-15] water technique. Pictures consisted of real world scenes with aversive, positive, and nonaversive content. Eye movements were recorded simultaneous with scan acquisition. Positron emission tomography images were analyzed for baseline, tonic activity, in addition to phasic changes ('activation') to salient stimuli. Lateral eye movement measures and on-line ratings showed good behavioral compliance with the task. Patients with schizophrenia showed impaired neural responses to salient stimuli in the right ventral striatum (VS), and they exhibited elevated tonic activity levels in the right VS and bilateral amygdala, inversely correlated with overall symptom severity. The patients also showed reduced modulation of visual cortex by salient stimuli. The results show that patients with schizophrenia exhibit impaired neural responses to emotionally salient stimuli in the VS, supporting a role for this structure in the pathophysiology of the illness. Reduced modulation of visual cortex by emotionally salient stimuli also suggests a failure to organize cerebral activity at a global level.

Adolescent↗