Prediction in the timing of pursuit eye movement initiation revealed by cross-axis vestibular–pursuit training in monkeys

The smooth-pursuit system interacts with the vestibular system to maintain the image of a moving target on the fovea. Efficient tracking performance requires information about the velocity and the initiation of target motion. Previous studies in monkeys have shown that training with orthogonal pursuit and whole body rotation results in adapted eye movement direction during chair rotation. In addition, the latency of the pursuit shortens and initial eye velocity increases in a task-dependent manner. To examine whether these adapted eye movements are predictive pursuit, we studied whether our monkeys could predict the timing of smooth eye movement initiation during chair rotation. Two young Japanese monkeys were rotated horizontally in a trapezoidal waveform (20°/s, ±10°) with random inter-trial intervals. A laser spot was moved vertically with the same trajectory at a constant delay ranging from 100 to 700 ms after the onset of the chair motion. The monkeys were required to pursue the spot. After this training, the latencies of pursuit eye movements following the onset of chair motion were examined in the presence of the target motion. The target was also briefly (for 500–700 ms) extinguished at 80 ms after the onset of chair rotation. Pursuit eye movements after training were initiated before the onset of target motion and the latencies were proportional to the delays used for training. The latencies and response magnitudes of pursuit with or without target blanking were similar. The auditory–pursuit training did not induce an initial pursuit response similar to that induced by vestibular–pursuit training. These results indicate that smooth eye movements during the chair rotation after the vestibular–pursuit training included a predictive pursuit component. The monkeys’ estimate of the delays revealed by the latencies of pursuit was shorter by 22–36% than the actual delays.     

Head–eye interactions during vertical gaze shifts made by rhesus monkeys

Changing the direction of the line of sight (gaze) can involve coordinated movements of the eyes and head. During gaze shifts directed along the horizontal meridian, the contribution of the eyes and head depends upon the position of the eyes in the orbits; the contribution of the head to accomplishing the overall shift in gaze declines as the eyes increasingly are deviated away from the direction of the ensuing gaze shift. Also during horizontal gaze shifts, changes in the metrics and kinematics of the saccadic (eye movement) portion of coordinated movements, are correlated with the amplitude and velocity of the concurrent head movement. With increasing head contributions, saccade peak velocities decline, durations increase and velocity profiles develop two peaks. It remains unknown whether the interaction between head and eyes observed during horizontal gaze shifts also occurs during vertical gaze shifts. Yet, a full understanding of the neural control of eye–head coordination will depend upon the correlation of neural activity and features of vertical as well as horizontal movements. This report describes the metrics and kinematics of vertical gaze shifts made by head-unrestrained rhesus monkeys. Key observations include: (1) during vertical gaze shifts of a particular amplitude, relative eye and head contributions depend upon the initial vertical positions of the eyes in the orbits; (2) as head contribution increases, peak eye velocities decline, durations increase and vertical velocity profiles develop two peaks; (3) head movement metrics and kinematics are accurately predictable given knowledge only of head movement amplitude. In these ways, vertical gaze shifts were found to be qualitatively similar to horizontal gaze shifts. It seems probable that similar mechanisms mediate head–eye interactions during both horizontal and vertical movements. These observations are consistent with the hypothesis that a signal proportional to vertical head velocity reduces the gain of the vertical saccade burst generator.     

Overlapping gaze shifts reveal timing of an eye–head gate

The ability to dissociate eye movements from head movements is essential to animals with foveas and fovea-like retinal specializations, as these species shift the eyes constantly, and moving the head with each gaze shift would be impractical and energetically wasteful. The processes by which the dissociation is effected remain unclear. We hypothesized that the dissociation is accomplished by means of a neural gate, which prevents a common gaze-shift command from reaching the neck circuitry when eye-only saccades are desired. We further hypothesized that such a gate would require a finite period to reset following opening to allow a combined eye–head saccade, and thus the probability of generating a head movement during a saccade would be augmented when a new visual target (the ‘test’ target) appeared during, or soon after, a combined eye–head saccade made to an earlier, ‘conditioning’ target. We tested human subjects using three different combinations of targets—a horizontal conditioning target followed by a horizontal test target (H/H condition), horizontal conditioning followed by vertical test (H/V), and vertical conditioning followed by horizontal test (V/H). We varied the delay between the onset of the conditioning head movement and the presentation of the test target, and determined the probability of generating a head movement to the test target as a function of target delay. As predicted, head movement probability was elevated significantly at the shortest target delays and declined thereafter. The half-life of the increase in probability averaged 740, 490, and 320 ms for the H/H, H/V, and V/H conditions, respectively. For the H/H condition, the augmentation appeared to outlast the duration of the conditioning head movement. Because the augmentation could outlast the conditioning head movement and did not depend on the head movements to the conditioning and test targets lying in the same directions, we could largely exclude the possibility that the augmentation arises from mechanical effects. These results support the existence of the hypothetical eye–head gate, and suggest ways that its constituent neurons might be identified using neurophysiological methods.     

Idiosyncratic variations in eye–head coupling observed in the laboratory also manifest during spontaneous behavior in a natural setting

The tendency to generate head movements during saccades varies from person to person. Head movement tendencies can be measured as subjects fixate sequences of illuminated targets, but the extent to which such measures reflect eye–head coupling during more natural behaviors is unknown. We quantified head movement tendencies in 20 normal subjects in a conventional laboratory experiment and in an outdoor setting in which the subjects directed their gaze spontaneously. In the laboratory, head movement tendencies during centrifugal saccades could be described by the eye-only range (EOR), customary ocular motor range (COMR), and the customary head orientation range (CHOR). An analogous EOR, COMR, and CHOR could be extracted from the centrifugal saccades executed in the outdoor setting. An additional six measures were introduced to describe the preferred ranges of eyes-in-head and head-on-torso manifest throughout the outdoor recording, i.e., not limited to the orientations following centrifugal saccades. These 12 measured variables could be distilled by factor analysis to one indoor and six outdoor factors. The factors reflect separable tendencies related to preferred ranges of visual search, head eccentricity, and eye eccentricity. Multiple correlations were found between the indoor and outdoor factors. The results demonstrate that there are multiple types of head movement tendencies, but some of these influence behavior across rather different experimental settings and tasks. Thus behavior in the two settings likely relies on common neural mechanisms, and the laboratory assays of head movement tendencies succeed in probing the mechanisms underlying eye–head coupling during more natural behaviors.

Pituitary–adrenal responses to arm versus leg exercise in untrained man

The purpose of this study was to examine pituitary–adrenal (PA) hormone responses [beta-endorphin (β-END), adrenocorticotropic hormone (ACTH) and cortisol] to arm exercise (AE) and leg exercise (LE) at 60 and 80% of the muscle-group specific VO₂ peak. Eight healthy untrained men (AE VO₂ peak=32.4±3.0 ml kg⁻¹ min⁻¹, LE VO₂ peak=46.9±5.3 ml kg⁻¹ min⁻¹) performed two sub-maximal AE and LE tests in random order. Plasma β-END, ACTH and cortisol were not different (P>0.05) between AE and LE at either exercise intensity; the 60% testing elicited no changes from pre-exercise (PRE) values. For 80% testing, plasma β-END, ACTH and cortisol were consistently, but not significantly, greater during LE than AE. In general, plasma β-END and ACTH were higher (P<0.05) during 80% exercise, than PRE, for both AE and LE. Plasma cortisol was elevated (P<0.05) above PRE during 80% LE, and following 80% for both AE and LE. Plasma ACTH was higher (P<0.05) during 80% LE and AE versus 60% LE and AE, respectively. Plasma β-END and cortisol were significantly higher during and immediately after 80% LE than 60% LE. Thus, plasma β-END, ACTH and cortisol responses were similar for AE and LE at the two relative exercise intensities, with the intensity threshold occurring somewhere between 60 and 80% of VO₂ peak. It appears that the smaller muscle mass associated with AE was sufficient to stimulate these PA axis hormones in a manner similar to LE, despite the higher metabolic stress (i.e., plasma La^-) associated with LE.     

Discharge of pursuit-related neurons in the caudal part of the frontal eye fields in juvenile monkeys with up–down pursuit asymmetry

The smooth-pursuit system uses retinal image-slip-velocity information of target motion to match eye velocity to actual target velocity. The caudal part of the frontal eye fields (FEF) contains neurons whose activity is related to direction and velocity of smooth-pursuit eye movements (pursuit neurons), and these neurons are thought to issue a pursuit command. During normal pursuit in well-trained adult monkeys, a pursuit command is usually not differentiable from the actual eye velocity. We examined whether FEF pursuit neurons signaled the actual eye velocity during pursuit in juvenile monkeys that exhibited intrinsic differences between upward and downward pursuit capabilities. Two, head-stabilized Japanese monkeys of 4 years of age were tested for sinusoidal vertical pursuit of target motion at 0.2–1.2 Hz (±10°, peak target velocity 12.5–75.0°/s). Gains of downward pursuit were 0.8–0.9 at 0.2–1.0 Hz, and peak downward eye velocity increased up to ~60°/s linearly with target velocity, whereas peak upward eye velocity saturated at 15–20°/s. The majority of downward FEF pursuit neurons increased the amplitude of their discharge modulation almost linearly up to 1.2 Hz. The majority of upward FEF pursuit neurons also increased amplitude of modulation nearly linearly as target frequency increased, and the regression slope was similar to that of downward pursuit neurons despite the fact that upward peak eye velocity saturated at ~0.5 Hz. These results indicate that the responses of the majority of upward FEF pursuit neurons did not signal the actual eye velocity during pursuit. We suggest that their activity reflected primarily the required eye velocity.     

Eye–head coordination in the guinea pig I. Responses to passive whole-body rotations

Vestibular reflexes act to stabilize the head and eyes in space during locomotion. Head stability is essential for postural control, whereas retinal image stability enhances visual acuity and may be essential for an animal to distinguish self-motion from that of an object in the environment. Guinea pig eye and head movements were measured during passive whole-body rotation in order to assess the efficacy of vestibular reflexes. The vestibulo-ocular reflex (VOR) produced compensatory eye movements with a latency of ~7 ms that compensated for 46% of head movement in the dark and only slightly more in the light (54%). Head movements, in response to abrupt body rotations, also contributed to retinal stability (21% in the dark; 25% in the light) but exhibited significant variability. Although compensatory eye velocity produced by the VOR was well correlated with head-in-space velocity, compensatory head-on-body speed and direction were variable and poorly correlated with body speed. The compensatory head movements appeared to be determined by passive biomechanical (e.g., inertial effects, initial tonus) and active mechanisms (the vestibulo-collic reflex or VCR). Chemically induced, bilateral lesions of the peripheral vestibular system abolished both compensatory head and eye movement responses.     

You don’t like me,do you? Enhanced ERP responses to averted eye gaze in social anxiety

Social anxiety is associated with an attentional bias toward angry and fearful faces, along with an enhanced processing of faces per se. However, little is known about the processing of gaze direction, a subtle but important social cue. Participants with high or low social anxiety (HSA/LSA) observed eye pairs with direct or averted gaze while subjective ratings and event-related potentials (ERPs) were measured. Behaviorally, all participants rated averted gaze as more unpleasant than direct gaze. Neurally, only HSA participants showed a trend for higher P100 amplitudes to averted gaze and significantly enhanced processing at late latencies (Late positive potential [LPP]), indicative of a specific processing bias for averted gaze. Furthermore, HSA individuals showed enhanced processing of both direct and averted gaze relative to the LSA group at intermediate latencies (Early posterior negativity [EPN]). Both general and specific attentional biases play a role in social anxiety. Averted gaze - a potential sign of disinterest - deserves more attention in the attentional bias literature.     

Face–to–face interactions between mothers and female infants in wild bearded capuchin monkeys (Sapajus libidinosus)

Once considered uniquely human, mother–infant face–to–face interactions (FF) were observed in a few captive primates. In these studies, FF were correlated to physical contact suggesting a mechanism mediating proximity between mother and infant, as is the case for humans. We investigated this hypothesis in wild capuchin monkeys (Sapajus libidinosus) during the first year of life of eight female infants. Data were weekly focal-day videos of infants from which we recorded FF with mothers. We expected FF would increase with infants’ age (as time in contact with mothers decreased) and would more likely occur in the absence of physical contact between the dyad. There was no effect of age in the proportion of interaction time spent in FF, nor in types of FF. A quarter of FF episodes occurred in the absence of physical contact between the dyad, and in most of them physical contact was resumed following the FF. Contrary to predictions, the stability in the first year, mainly when mothers–female infants were in contact, indicates that FF act primarily promoting opportunities for affective communication and intuitive care. However, we found some supportive evidence for the hypothesis that FF regulate proximity between mother and infant, mainly in resume physical contact.     

Development of head movement propensity in 4–15 year old children in response to visual step stimuli

Head movement frequency of children in response to horizontal step stimulus is investigated. The aim is to determine if there is a correlation between the age of the child and the frequency of head movements made to visual step stimuli presented at a fixed distance. Also of importance is whether there is a period of rapid change in the frequency of head movements, and if so, what factors could be influencing this change. Seventy-three participants, between the ages of 4 and 15 years were requested to “look at a spot of light” in response to step stimuli which varied in size from 5 to 60°. Eye and head movements were recorded with a video based eye tracker (EL-Mar 2020) equipped with a Flock of Birds head tracker. Frequency of head movements was calculated for each participant and averaged across participants for each age group. Average head movement frequency was then plotted as a function of age. The frequency and variability of head movements decreases as a function of age. This decrease is linear between the ages of 4 and 15 years (y = −1.465x + 22.58; R ² = 0.4378; F = 26.48; P < 0.0001). More head movements are made in response to larger step sizes than to smaller ones for all ages. The gradual decrease in frequency of head movements in response to step stimuli suggests that a specific environmental event, such as reading, is not the cause of the decline. Improved efficiency of eye movements could be due to pre-programmed factors related to neurological development. Alternatively, cognitive factors may be involved. Children may actually learn that utilizing their head for gaze shifts is more energy and time consuming, than merely using the eyes alone.     

Functional imaging of changes in cerebellar activity related to learning during a novel eye–hand tracking task

Coordination between the eyes and the hand is likely to be based on a process of motor learning, so that the interactions between the two systems can be accurately controlled. By using an unusual tracking task we measured the change in brain activation levels, as recorded with 3T functional magnetic resonance imaging (fMRI), between naïve human subjects and the same subjects after a period of extended training. Initially the performance of the two groups was similar. One subject group was then trained in a synchronous, coordinated, eye–hand task; the other group trained with a 304 ms temporal offset between hand and eye tracking movements. After training, different patterns of performance were observed for the groups, and different functional activation profiles. Significant change in the relationship between functional activation levels and eye–hand task conditions was predominantly restricted to visuo-motor areas of the lateral and vermal cerebellum. In an additional test with one of the subject groups, we show that there was increased cerebellar activation after learning, irrespective of change in performance error. These results suggest that two factors contribute to the measured blood oxygen level-dependent (BOLD) signal. One declined with training and may be directly related to performance error. The other increased after training, in the test conditions nearest to the training condition, and may therefore be related to acquisition of experience in the task. The loci of activity changes suggest that improved performance is because of selective modified processing of ocular and manual control signals within the cerebellum. These results support the suggestion that coordination between eye and hand movement is based on an internal model acquired by the cerebellum that provides predictive signals linking the control of the two effectors.     

Active versus passive transportation to school–differences in screen time,socio-economic position and perceived environmental characteristics in adolescent girls

Objective: The aims of this study were (1) to assess the relationships between transport to and from school (active vs. passive), sedentary behaviours, measures of socio-economic position and perceived environmental variables, and (2) to determine which, if any, variables were predictors of active transportation.

Methods: The sample comprised 705 girls with mean age of 14.7 (SD?=?1.6) years old. Questionnaires were used to describe travel mode to school and to estimate weekly television and computer use (screen time). Girls were assigned to active transportation (AT) or passive transportation (PT) groups depending on whether they walked or bicycled (AT) to and from school or travelled by car or bus (PT). Screen time was determined by the number of hours they reported watching television and using computers in the week preceding the examination, including weekends. Socio-economic position was established by parental occupation and educational level. A questionnaire assessed Perceived Neighbourhood Environments.

Results: No statistically significant differences were seen for screen time between travel groups. Occupational status of both mother (r?=??0.17) and father (r?=??0.15) and father's educational level (r?=??0.10) were significantly and negatively associated with AT, while street connectivity (r?=?0.10) was positively and significantly associated with AT. Logistic regression analysis showed that the likelihood of active commuting decreased by around 50% with increasing father's occupation (odds ratio (OR)?=?0.51; p?≤?0.05) and father's education (OR?=?0.52; p?≤?0.05) from low to middle socio-economic position groups. Further, the data showed that girls who agreed that ‘there are many four-way intersections in my neighbourhood’ were more likely to be active (OR?=?1.63; p?≤?0.05).

Conclusion: The data of this study showed that lower socio-economic position is associated with active commuting to school and that street connectivity is a predictor of active transportation in adolescent girls.     

Walk–run transition in young and older adults: with special reference to the cardio-respiratory responses

Cardio-respiratory responses of young and older subjects performing walking and running protocols at the walk–run transition speed (WRT) were compared. A total of 26 volunteers assigned to younger (YG, 24 ± 3 years) and older (OG, 64 ± 6 years) groups underwent a protocol to determine the WRT used in 6-min walking and running protocols. Oxygen uptake (VO₂), ventilation (V _E), expired carbon dioxide (VCO₂), heart rate (HR) and perceived exertion (RPE) were assessed. Oxygen pulse (O₂ pulse) and respiratory exchange ratio (RER) were calculated. The WRT was not different between groups (OG: 6.84 ± 0.69 km h⁻¹ vs. YG: 7.04 ± 0.77 km h⁻¹, P = 0.62). No between-group differences were found within a given gait pattern for VO₂ (P = 0.061) and VCO₂ (P = 0.076). However, VO₂ (P = 0.0022) and VCO₂ (P = 0.0041) increased in OG when running, remaining stable in YG (VO₂: P = 0.622; VCO₂: P = 0.412). The VE was higher in OG compared to YG in walking (P = 0.030) and running (P = 0.004) protocols. No age-related (P = 0.180) or locomotion (P = 0.407) effects were found for RER. The HR increased in OG and between-group difference was detected while running (P = 0.003). No within- (P = 0.447) or between-group (P = 0.851) difference was found for O₂ pulse. The net VO₂ increased from walking to running in OG (P < 0.0001) but not in YG (P = 0.53), while RPE was lower in YG (P = 0.041) but stable in OG (P = 0.654). In conclusion, the WRT speed was similar across the age groups. However, the VO₂ and VCO₂ increase from walking to running was larger for OG than YG. The HR, VE and RPE were also higher when running in OG compared to YG. Therefore, the locomotion strategy had different impacts on the metabolic demand of older and younger subjects.     

Viral outcome of simian–human immunodeficiency virus SHIV-89.6P adapted to cynomolgus monkeys

Simian–human immunodeficiency virus (SHIV) 89.6P is considered to be one of the most pathogenic chimeric viruses in rhesus macaques. However, when crossing from one to another species of monkeys the pathogenicity of this virus may be affected. By using SHIV-89.6P_cy243, a virus obtained by passaging SHIV-89.6P in cynomolgus macaques, we investigated the dynamics of viral replication and the impact of the inoculum size (from 10 up to 50 monkey infectious dose) on the progression of the infection in 22 cynomolgus macaques. SHIV-89.6P_cy243 caused massive depletion of CD4+ T-cells within 4 weeks of the inoculum, followed by an irreversible immune deficiency in a high proportion of the infected monkeys. This study demonstrates that SHIV-89.6P_cy243 is pathogenic in cynomolgus macaques and that the dynamics of the viral replication and the rate of clinical progression depend on the size of the inoculum. Our findings provide unique and relevant data, particularly with regard to the value of the in vivo titration used to select the most appropriate infectious dose to study the “virus-host” interplay. Nucleotide sequences data reported are available in the GenBank databases under the accession numbers U89134; AF217181; EF672090.     

Target selection in eye–hand coordination: Do we reach to where we look or do we look to where we reach?

During a goal-directed movement of the hand to a visual target the controlling nervous system depends on information provided by the visual system. This suggests that a coupling between these two systems is crucial. In a choice condition with two or more equivalent objects present at the same time the question arises whether we (a) reach for the object we have selected to look at or (b) look to the object we have selected to grasp. Therefore, we examined the preference of human subjects selecting the left or the right target and its correlation to the action to be performed (eye-, arm- or coordinated eye–arm movement) as well as the horizontal position of the target. Two targets were presented at the same distance to the left and right of a fixation point and the stimulus onset asynchrony (SOA) was adjusted until both targets were selected equally often. This balanced SOA was then taken as a quantitative measure of selection preference. We compared these preferences at three horizontal positions for the different movement types (eye, arm, both). The preferences of the ‘arm’ and ‘coordinated eye–arm’ movement types were correlated more strongly than the preferences of the other movement types. Thus, we look to where we have already selected to grasp. These findings provide evidence that in a coordinated movement of eyes and arm the control of gaze is a means to an end, namely a tool to conduct the arm movement properly.     

Regional characteristics of electrical responses (in the band 1–225 Hz) in the cerebral cortex to conditioned stimuli in operant conditioning

Power spectra of short-term (less than 1 sec) electrical responses to conditioned stimuli were studied over the frequency range 1–225 Hz in dogs during food-related operant conditioning. These spectra demonstrated regional characteristics in terms of energy levels and frequency composition. Responses were more marked in the visual and parietal areas of the left hemisphere. Power in responses to a differential stimulus were significantly lower than with responses to positive stimuli, mainly because of the high-frequency range (80–225 Hz); energy levels in these two situations were similar during prestimulus intervals. The frequency composition of responses was defined by a series of discrete frequencies in the gamma (30–80 Hz) and high-frequency ranges. __________ Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 55, No. 5, pp. 658–670, September–October, 2005.     

Optimization of SSVEP brain responses with application to eight-command Brain–Computer Interface

This study pursues the optimization of the brain responses to small reversing patterns in a Steady-State Visual Evoked Potentials (SSVEP) paradigm, which could be used to maximize the efficiency of applications such as Brain–Computer Interfaces (BCI). We investigated the SSVEP frequency response for 32 frequencies (5–84 Hz), and the time dynamics of the brain response at 8, 14 and 28 Hz, to aid the definition of the optimal neurophysiological parameters and to outline the onset-delay and other limitations of SSVEP stimuli in applications such as our previously described four-command BCI system. Our results showed that the 5.6–15.3 Hz pattern reversal stimulation evoked the strongest responses, peaking at 12 Hz, and exhibiting weaker local maxima at 28 and 42 Hz. After stimulation onset, the long-term SSVEP response was highly non-stationary and the dynamics, including the first peak, was frequency-dependent. The evaluation of the performance of a frequency-optimized eight-command BCI system with dynamic neurofeedback showed a mean success rate of 98%, and a time delay of 3.4 s. Robust BCI performance was achieved by all subjects even when using numerous small patterns clustered very close to each other and moving rapidly in 2D space. These results emphasize the need for SSVEP applications to optimize not only the analysis algorithms but also the stimuli in order to maximize the brain responses they rely on.     

Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena

The individual properties of visual objects, like form or color, are represented in different areas in our visual cortex. In order to perceive one coherent object, its features have to be bound together. This was found to be achieved in cat and monkey brains by temporal correlation of the firing rates of neurons which code the same object. This firing rate is predominantly observed in the gamma frequency range (approx. 30–80 Hz, mainly around 40 Hz). In addition, it has been shown in humans that stimuli which flicker at gamma frequencies are processed faster by our brains than when they flicker at different frequencies. These effects could be due to neural oscillators, which preferably oscillate at certain frequencies, so-called resonance frequencies. It is also known that neurons in visual cortex respond to flickering stimuli at the frequency of the flickering light. If neural oscillators exist with resonance frequencies, they should respond more strongly to stimulation with their resonance frequency. We performed an experiment, where ten human subjects were presented flickering light at frequencies from 1 to 100 Hz in 1-Hz steps. The event-related potentials exhibited steady-state oscillations at all frequencies up to at least 90 Hz. Interestingly, the steady-state potentials exhibited clear resonance phenomena around 10, 20, 40 and 80 Hz. This could be a potential neural basis for gamma oscillations in binding experiments. The pattern of results resembles that of multiunit activity and local field potentials in cat visual cortex. Electronic Publication