scholarly journals Eye movements as a readout of sensorimotor decision processes

2019 ◽  
Author(s):  
Jolande Fooken ◽  
Miriam Spering

AbstractReal-world tasks, such as avoiding obstacles, require a sequence of interdependent decisions to reach accurate motor outcomes. Yet, most studies on primate decision making involve simple one-step choices. Here we investigate how sensorimotor decisions develop over time. In a go/no-go interception task human observers (n=42) judged whether a briefly-presented moving target would pass (interception required) or miss (no hand movement required) a strike box while their eye and hand movements were recorded. Go/no-go decision formation had to occur within the first few hundred milliseconds to allow time-critical interception. We found that the earliest time point at which eye movements started to differentiate decision outcome (go vs. no-go) coincided with hand movement onset. Moreover, eye movements were related to different stages of decision making. Whereas higher eye velocity during smooth pursuit initiation (prior to “whether” decision) was related to higher go/no-go decision accuracy, faster pursuit maintenance was associated with accurate interception timing (“when” decision). These results indicate that pursuit initiation and maintenance are continuously linked to ongoing sensorimotor decision formation.


2020 ◽  
Vol 123 (4) ◽  
pp. 1439-1447
Author(s):  
Jolande Fooken ◽  
Miriam Spering

Real-world tasks, such as avoiding obstacles, require a sequence of interdependent choices to reach accurate motor actions. Yet, most studies on primate decision making involve simple one-step choices. Here we analyze motor actions to investigate how sensorimotor decisions develop over time. In a go/no-go interception task human observers ( n = 42) judged whether a briefly presented moving target would pass (interceptive hand movement required) or miss (no hand movement required) a strike box while their eye and hand movements were recorded. Go/no-go decision formation had to occur within the first few hundred milliseconds to allow time-critical interception. We found that the earliest time point at which eye movements started to differentiate actions (go versus no-go) preceded hand movement onset. Moreover, eye movements were related to different stages of decision making. Whereas higher eye velocity during smooth pursuit initiation was related to more accurate interception decisions (whether or not to act), faster pursuit maintenance was associated with more accurate timing decisions (when to act). These results indicate that pursuit initiation and maintenance are continuously linked to ongoing sensorimotor decision formation. NEW & NOTEWORTHY Here we show that eye movements are a continuous indicator of decision processes underlying go/no-go actions. We link different stages of decision formation to distinct oculomotor events during open- and closed-loop smooth pursuit. Critically, the earliest time point at which eye movements differentiate actions preceded hand movement onset, suggesting shared sensorimotor processing for eye and hand movements. These results emphasize the potential of studying eye movements as a readout of cognitive processes.



2019 ◽  
Author(s):  
Stuart Behling ◽  
Stephen G. Lisberger

AbstractSmooth pursuit eye movements are used by primates to track moving objects. They are initiated by sensory estimates of target speed represented in the middle temporal (MT) area of extrastriate visual cortex and then supported by motor feedback to maintain steady-state eye speed at target speed. Here, we show that reducing the coherence in a patch of dots for a tracking target degrades the eye speed both at the initiation of pursuit and during steady-state tracking, when eye speed reaches an asymptote well below target speed. The deficits are quantitatively different between the motor-supported steady-state of pursuit and the sensory-driven initiation of pursuit, suggesting separate mechanisms. The deficit in visually-guided pursuit initiation could not explain the deficit in steady-state tracking. Pulses of target speed during steady-state tracking revealed lower sensitivities to image motion across the retina for lower values of dot coherence. However, sensitivity was not zero, implying that visual motion should still be driving eye velocity towards target velocity. When we changed dot coherence from 100% to lower values during accurate steady-state pursuit, we observed larger eye decelerations for lower coherences, as expected if motor feedback was reduced in gain. A simple pursuit model accounts for our data based on separate modulation of the strength of visual-motor transmission and motor feedback. We suggest that reduced dot coherence creates less reliable target motion that impacts pursuit initiation by changing the gain of visual-motor transmission and perturbs steady-state tracking by modulation of the motor corollary discharges that comprise eye velocity memory.



2007 ◽  
Vol 97 (1) ◽  
pp. 761-771 ◽  
Author(s):  
Uwe J. Ilg ◽  
Stefan Schumann

The contributions of the middle superior temporal area (MST) in the posterior parietal cortex of rhesus monkeys to the generation of smooth-pursuit eye movements as well as the contributions to motion perception are well established. Here, we present the first experimental evidence that this area also contributes to the generation of goal-directed hand movements toward a moving target. This evidence is based on the outcome of intracortical microstimulation experiments and transient lesions by small injections of muscimol at identified sites within the lateral part of area MST (MST-l). When microstimulation was applied during the execution of smooth-pursuit eye movements, postsaccadic eye velocity in the direction of the preferred direction of the stimulated site increased significantly (in 93 of 136 sites tested). When microstimulation was applied during a hand movement trial, the hand movement was displaced significantly in the same direction (in 28 of 39 sites tested). When we lesioned area MST-l transiently by injections of muscimol, steady-state eye velocity was exclusively reduced for ipsiversive smooth-pursuit eye movements. In contrast, hand movements were displaced toward the contralateral side, irrespective of the direction of the moving target. Our results provide evidence that area MST-l is involved in the processing of moving targets and plays a role in the execution of smooth-pursuit eye movements as well as visually guided hand movements.



2001 ◽  
Vol 86 (5) ◽  
pp. 2413-2425 ◽  
Author(s):  
M. Missal ◽  
S. J. Heinen

The role of the supplementary eye fields (SEF) during smooth pursuit was investigated with electrical microstimulation. We found that stimulation in the SEF increased the acceleration and velocity of the eyes in the direction of target motion during smooth pursuit initiation but not during sustained pursuit. The increase in eye velocity during initiation will be referred to as pursuit facilitation and was observed at sites where saccades could not be evoked with the same stimulation parameters. On average, electrical stimulation increased eye velocity by ∼20%. At most sites, the threshold for a significant facilitation was 50 μA with a stimulation frequency of 300 Hz. Facilitation of pursuit initiation depended on the timing of stimulation trains. The effect was most pronounced if the stimulation was delivered before smooth pursuit initiation. On average, eye velocity in stimulation trials increased linearly as a function of eye velocity in control trials, and this function had a slope greater than one, suggesting a multiplicative influence of the stimulation. Stimulation during a fixation task did not evoke smooth eye movements. The latency of catch-up saccades was increased during facilitation, but their accuracy was not affected. Saccades toward stationary targets were not affected by the stimulation. The results are further evidence that the SEF plays a role in smooth pursuit in addition to its known role in saccade planning and suggest that this role may be to control the gain of smooth pursuit during initiation. The covariance between pursuit facilitation and the timing of the catch-up saccade as a result of stimulation suggests that these different eye movements systems are coordinated to achieve a common goal.



1995 ◽  
Vol 74 (3) ◽  
pp. 1367-1372 ◽  
Author(s):  
G. Cheron ◽  
S. Saussez ◽  
N. Gerrits ◽  
E. Godaux

1. Properties of nucleus incertus (NIC) neurons projecting to the cerebellar flocculus were studied in alert cats by using chronic unit and eye movement recording and antidromic activation. Projection of these neurons onto the flocculus was verified with retrograde transport of horseradish peroxidase after injections in the flocculus. 2. Bipolar stimulation electrodes were implanted into the "middle" zone of each flocculus because this zone is known to be involved in the control of horizontal eye movements. The dorsomedial aspect of the pontine tegmentum was explored with microelectrodes during stimulation of both flocculi. The majority of neurons antidromically activated from the flocculus were found in the caudal part of the NIC. 3. Of the 69 neurons activated from the flocculus, 44 were classified as burst-tonic (BT) neurons; 34 discharged in relation with horizontal movements of the eye, 10 in relation with vertical movements. Of the 14 remaining neurons, 6 were not related to eye movements and 8 were classified as burst neurons. The BT neurons of the NIC displayed a great sensitivity to both horizontal eye position and horizontal eye velocity. 4. This study demonstrates the presence of a new group of horizontal eye movement related BT neurons situated in the NIC. The fact that they project to the horizontal floccular zone emphasizes the importance of the functional specialization of the different Purkinje cell zones.



Author(s):  
Charles H. Hammer ◽  
Seymour Ringel

Sixty subjects worked a series of sequential decision making tasks in which the amount of information provided and feedback of results were the independent variables. Data were collected on decision accuracy, confidence in decision accuracy, and judged sufficiency of the information provided. Accuracy, confidence in accuracy, and ratings of sufficiency increased as amount of information provided was increased. Feedback produced increases in decision accuracy only. For forty percent of all correct responses, subjects judged the information provided to be insufficient as a basis for taking action. These data strongly suggest that lack of confidence in their ability to make accurate decisions may cause some decision makers to delay taking action even when they are able to make an accurate decision on the basis of the information available.



1998 ◽  
Vol 80 (1) ◽  
pp. 28-47 ◽  
Author(s):  
Masaki Tanaka ◽  
Kikuro Fukushima

Tanaka, Masaki and Kikuro Fukushima. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80: 28–47, 1998. To examine how the periarcuate area is involved in the control of smooth pursuit eye movements, we recorded 177 single neurons while monkeys pursued a moving target in the dark. The majority (52%, 92/177) of task-related neurons responded to pursuit but had little or no response to saccades. Histological reconstructions showed that these neurons were located mainly in the posterior bank of the arcuate sulcus near the sulcal spur. Twenty-seven percent (48/177) changed their activity at the onset of saccades. Of these, 36 (75%) showed presaccadic burst activity with strong preference for contraversive saccades. Eighteen (10%, 18/177) were classified as eye-position–related neurons, and 11% (19/177) were related to other aspects of the stimuli or response. Among the 92 neurons that responded to pursuit, 85 (92%) were strongly directional with uniformly distributed preferred directions. Further analyses were performed in these directionally sensitive pursuit-related neurons. For 59 neurons that showed distinct changes in activity around the initiation of pursuit, the median latency from target motion was 96 ms and that preceding pursuit was −12 ms, indicating that these neuron can influence the initiation of pursuit. We tested some neurons by briefly extinguishing the tracking target ( n = 39) or controlling its movement with the eye position signal ( n = 24). The distribution of the change in pursuit-related activity was similar to previous data for the dorsomedial part of the medial superior temporal neurons ( Newsome et al. 1988) , indicating that pursuit-related neurons in the periarcuate area also carry extraretinal signals. For 22 neurons, we examined the responses when the animals reversed pursuit direction to distinguish the effects of eye acceleration in the preferred direction from oppositely directed eye velocity. Almost all neurons discharged before eye velocity reached zero, however, only nine neurons discharged before the eyes were accelerated in the preferred direction. The delay in neuronal responses relative to the onset of eye acceleration in these trials might be caused by suppression from oppositely directed pursuit velocity. The results suggest that the periarcuate neurons do not participate in the earliest stage of eye acceleration during the change in pursuit direction, although most of them may participate in the early stages of pursuit initiation in the ordinary step-ramp pursuit trials. Some neurons changed their activity when the animals fixated a stationary target, and this activity could be distinguished easily from the strong pursuit-related responses. Our results suggest that the periarcuate pursuit area carries extraretinal signals and affects the premotor circuitry for smooth pursuit.



1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen

The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement–based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + rE˙, where FR is firing rate, E and E˙ are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or “slide” (FR = b + kE + rE˙ + uË − c[Formula: see text]), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients ( r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias ( b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.



1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs

1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the “marginal zone”). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral “on” directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)



Autism ◽  
2019 ◽  
Vol 24 (3) ◽  
pp. 730-743 ◽  
Author(s):  
Emma Gowen ◽  
Andrius Vabalas ◽  
Alexander J Casson ◽  
Ellen Poliakoff

This study investigated whether reduced visual attention to an observed action might account for altered imitation in autistic adults. A total of 22 autistic and 22 non-autistic adults observed and then imitated videos of a hand producing sequences of movements that differed in vertical elevation while their hand and eye movements were recorded. Participants first performed a block of imitation trials with general instructions to imitate the action. They then performed a second block with explicit instructions to attend closely to the characteristics of the movement. Imitation was quantified according to how much participants modulated their movement between the different heights of the observed movements. In the general instruction condition, the autistic group modulated their movements significantly less compared to the non-autistic group. However, following instructions to attend to the movement, the autistic group showed equivalent imitation modulation to the non-autistic group. Eye movement recording showed that the autistic group spent significantly less time looking at the hand movement for both instruction conditions. These findings show that visual attention contributes to altered voluntary imitation in autistic individuals and have implications for therapies involving imitation as well as for autistic people’s ability to understand the actions of others.



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