Martin Paré

Influence of history on saccade countermanding performance in humans and macaque monkeys

The stop-signal or countermanding task probes the ability to control action by requiring subjects to withhold a planned movement in response to an infrequent stop signal which they do with variable success depending on the delay of the stop signal. We investigated whether performance of humans and macaque monkeys in a saccade countermanding task was influenced by stimulus and performance history. In spite of idiosyncrasies across subjects several trends were evident in both humans and monkeys. Response time decreased after successive trials with no stop signal. Response time increased after successive trials with a stop signal. However, post-error slowing was not observed. Increased response time was observed mainly or only after cancelled (signal inhibit) trials and not after noncancelled (signal respond) trials. These global trends were based on rapid adjustments of response time in response to momentary fluctuations in the fraction of stop signal trials. The effects of trial sequence on the probability of responding were weaker and more idiosyncratic across subjects when stop signal fraction was fixed. However, both response time and probability of responding were influenced strongly by variations in the fraction of stop signal trials. These results indicate that the race model of countermanding performance requires extension to account for these sequential dependencies and provide a basis for physiological studies of executive control of countermanding saccade performance.

Gaze shifts evoked by stimulation of the superior colliculus in the head-free cat conform to the motor map but also depend on stimulus strength and fixation activity

In our previous paper we demonstrated that electrical microstimulation of the fixation area at the rostral pole of the cat superior colliculus (SC) elicits no gaze movement but, rather, transiently suppresses eye-head gaze saccades. In this paper, we investigated the more caudal region of the SC and its interaction with the fixation area. In the alert head-free cat, supra-threshold stimulation in the anterior portion of the SC but outside the fixation area evoked small saccadic shifts of gaze consisting mainly of an eye movement, the heads contribution being small. Stimulating more posteriorly elicited large gaze saccades consisting of an ocular saccade combined with a rapid head movement. At these latter stimulation sites, craniocentric (goal-directed) eye movements were evoked when the cats head was restrained. The amplitude of eye-head gaze saccades elicited at a particular stimulation site increased with stimulus duration, current strength, and pulse rate, until a constant or “unit” value was reached. The peak velocity of gaze shifts depended on both pulse rate and current strength. The movement direction was not affected by stimulus parameters. The unit gaze vector evoked, in the head-free condition, by stimulating one collicular site was similar to that coded by efferent neurons recorded at that site, thereby indicating a retinotopically coded gaze error representation on the collicular motor map which is not revealed by stimulating the head-fixed animal. Evoked gaze saccades were found to be influenced by fixation behavior. The amplitude of evoked gaze shifts was reduced if stimulation occurred when the hungry animal fixated a food target. Electrical activation of the collicular fixation area was found to mimic well the effects of natural fixation on evoked gaze shifts. Taken together, our results support the view that the overall distribution and level of collicular activity contributes to the encoding of the metrics of gaze saccades. We suggest that the combined levels of activity at the site being stimulated and at the fixation area influence the amplitude of evoked gaze saccades through competition. When stimulation is at low intensities, fixation-related activity reduces the amplitude of evoked gaze saccades. At high activation levels, the site being stimulated dominates and the gaze vector is specified only by that sites collicular output neurons, from which arises the close correspondence between the unit-evoked gaze saccades and the neurally coded gaze vector at that site.

The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons

The superior colliculus has long been recognized as an important structure in the generation of saccadic displacements of the visual axis. Neurons with presaccadic activity encoding saccade vectors are topographically organized and form a “motor map.” Recently, neurons with fixation-related activity have been recorded at the collicular rostral pole, at the area centralis representation or fixation area. Another collicular function which deals with the maintenance of fixation behavior by means of active inhibition of orientation commands was then suggested. We tested that hypothesis as it relates to the suppression of gaze saccades (gaze = eye in space = eye in head + head in space) in the head-free cat by increasing the activity of the fixation cells at the rostral pole with electrical microstimulation. Long stimulation trains applied before gaze saccades delayed their initiation. Short stimuli, delivered during the gaze saccades, transiently interrupted both eye and head components. These results provide further support for a role in fixation behavior for collicular fixation neurons. Brainstem omnipause neurons also exhibit fixation-related activity and have been shown to receive a direct excitatory input from the superior colliculus. To determine whether the collicular projection to omnipause neurons arises from the fixation area, the deep layers of the superior colliculus were electrically stimulated either at the rostral pole including the fixation area or in more caudal regions where stimulation evokes orienting responses. Forty-nine neurons were examined in three cats. 61% of the neurons were found to be orthodromically excited by single-pulse stimulation of the rostral pole, whereas only 29% responded to caudal stimulation. In addition, stimuli delivered to the rostral pole activated, on average, omnipause neurons at shorter latencies and with lower currents than those applied in caudal regions. These results suggest that excitatory inputs to omnipause neurons from the superior colliculus are principally provided by the fixation area, via which the superior colliculus could play a role in suppression of gaze shifts.

Retrograde labeling of neurons in the brain stem following injections of [3H]choline into the rat spinal cord

In an attempt to identify cholinergic neurons in the brain stem which project to the spinal cord, [3H]choline (100, 20, 10, 5 or 1 microCi) was injected into the upper cervical spinal cord in 55 rats. The animals were killed 20 h later and the brains processed for autoradiography of diffusible substances. At all doses of [3H]choline, cells were consistently, retrogradely labeled in the medical medullary reticular formation, the lateral vestibular nucleus, the dorsolateral pontine tegmentum and the red nucleus. The retrogradely labeled cells were found to be moderately to darkly stained for acetylcholinesterase. Injection of [3H]noradrenaline (50 microCi) into the upper cervical spinal cord resulted in retrograde labeling of cells in the locus coeruleus, subcoeruleus and the ventrolateral pontine tegmentum, that correspond in position to the neurons of the A6, A7 and A5 catecholamine cell groups, respectively. Injection of [3H]serotonin (20 microCi) into the upper cervical spinal cord was associated with retrograde labeling of cells in the raphe pallidus, obscurus and magnus nuclei that correspond in position to those of the B1, B2 and B3 serotonin cell groups, respectively. Injection of True Blue into the upper cervical spinal cord was followed by retrograde labeling of a large number of cells located in the areas where cells were retrogradely labeled by [3H]choline, [3H]noradrenaline and [3H]serotonin, and additionally, in the solitary tract nucleus, the lateral, parvicellular medullary reticular formation, the caudal and oral pontine reticular formation, the mesencephalic reticular formation and the superior colliculus. These results indicate that from the cervical spinal cord, [3H]choline selectively retrogradely labels a certain population of non-monaminergic, acetylcholinesterase-positive cells localized in the medial medullary, and secondarily the dorsolateral pontine, reticular formation, the lateral vestibular nucleus, and the red nucleus.

Signal transformations from cerebral cortex to superior colliculus for the generation of saccades.

The ability of primates to make rapid and accurate saccadic eye movements for exploring the natural world is based on a neuronal system in the brain that has been studied extensively and is known to include multiple brain regions extending throughout the neuraxis. We examined the characteristics of signal flow in this system by recording from identified output neurons of two cortical regions, the lateral intraparietal area (LIP) and the frontal eye field (FEF), and from neurons in a brainstem structure targeted by these output neurons, the superior colliculus (SC). We compared the activity of neurons in these three populations while monkeys performed a delayed saccade task that allowed us to quantify visual responses, motor activity, and intervening delay activity. We examined whether delay activity was related to visual stimulation by comparing the activity during interleaved trials when a target was either present or absent during the delay period. We examined whether delay activity was related to movement by using a Go/Nogo task and comparing the activity during interleaved trials in which a saccade was either made (Go) or not (Nogo). We found that LIP output neurons, FEF output neurons, and SC neurons can all have visual responses, delay activity, and presaccadic bursts; hence in this way they are all quite similar. However, the delay activity tended to be more related to visual stimulation in the cortical output neurons than in the SC neurons. Complementing this, the delay activity tended to be more related to movement in the SC neurons than in the cortical output neurons. We conclude, first, that the signal flow leaving the cortex represents activity at nearly every stage of visuomotor transformation, and second, that there is a gradual evolution of signal processing as one proceeds from cortex to colliculus.

Proactive Inhibitory Control and Attractor Dynamics in Countermanding Action: A Spiking Neural Circuit Model

Flexible behavior depends on the brains ability to suppress a habitual response or to cancel a planned movement whenever needed. Such inhibitory control has been studied using the countermanding paradigm in which subjects are required to withhold an imminent movement when a stop signal appears infrequently in a fraction of trials. To elucidate the circuit mechanism of inhibitory control of action, we developed a recurrent network model consisting of spiking movement (GO) neurons and fixation (STOP) neurons, based on neurophysiological observations in the frontal eye field and superior colliculus of behaving monkeys. The model places a premium on the network dynamics before the onset of a stop signal, especially the experimentally observed high baseline activity of fixation neurons, which is assumed to be modulated by a persistent top-down control signal, and their synaptic interaction with movement neurons. The model simulated observed neural activity and fit behavioral performance quantitatively. In contrast to a race model in which the STOP process is initiated at the onset of a stop signal, in our model whether a movement will eventually be canceled is determined largely by the proactive top-down control and the stochastic network dynamics, even before the appearance of the stop signal. A prediction about the correlation between the fixation neural activity and the behavioral outcome was verified in the neurophysiological data recorded from behaving monkeys. The proposed mechanism for adjusting control through tonically active neurons that inhibit movement-producing neurons has significant implications for exploring the basis of impulsivity associated with psychiatric disorders.

Spatial statistics of gaze fixations during dynamic face processing

Abstract Social interaction involves the active visual perception of facial expressions and communicative gestures. This study examines the distribution of gaze fixations while watching videos of expressive talking faces. The knowledge-driven factors that influence the selective visual processing of facial information were examined by using the same set of stimuli, and assigning subjects to either a speech recognition task or an emotion judgment task. For half of the subjects assigned to each of the tasks, the intelligibility of the speech was manipulated by the addition of moderate masking noise. Both tasks and the intelligibility of the speech signal influenced the spatial distribution of gaze. Gaze was concentrated more on the eyes when emotion was being judged as compared to when words were being identified. When noise was added to the acoustic signal, gaze in both tasks was more centralized on the face. This shows that subjects gaze is sensitive to the distribution of information on the face, but can also be influenced by strategies aimed at maximizing the amount of visual information processed.

Neural Basis of Adaptive Response Time Adjustment during Saccade Countermanding

Humans and macaque monkeys adjust their response time adaptively in stop-signal (countermanding) tasks, responding slower after stop-signal trials than after control trials with no stop signal. We investigated the neural mechanism underlying this adaptive response time adjustment in macaque monkeys performing a saccade countermanding task. Earlier research showed that movements are initiated when the random accumulation of presaccadic movement-related activity reaches a fixed threshold. We found that a systematic delay in response time after stop-signal trials was accomplished not through a change of threshold, baseline, or accumulation rate, but instead through a change in the time when activity first began to accumulate. The neurons underlying movement initiation have been identified with stochastic accumulator models of response time performance. Therefore, this new result provides surprising new insights into the neural instantiation of stochastic accumulator models and the mechanisms through which executive control can be exerted.

Gaze behavior in audiovisual speech perception: the influence of ocular fixations on the McGurk effect.

We conducted three experiments in order to examine the influence of gaze behavior and fixation on audiovisual speech perception in a task that required subjects to report the speech sound they perceived during the presentation of congruent and incongruent (McGurk) audiovisual stimuli. Experiment 1 showed that the subjects’ natural gaze behavior rarely involved gaze fixations beyond the oral and ocular regions of the talker’s face and that these gaze fixations did not predict the likelihood of perceiving the McGurk effect. Experiments 2 and 3 showed that manipulation of the subjects’ gaze fixations within the talker’s face did not influence audiovisual speech perception substantially and that it was not until the gaze was displaced beyond 10°–20° from the talker’s mouth that the McGurk effect was significantly lessened. Nevertheless, the effect persisted under such eccentric viewing conditions and became negligible only when the subject’s gaze was directed 60° eccentrically. These findings demonstrate that the analysis of high spatial frequency information afforded by direct oral foveation isnot necessary for the successful processing of visual speech information.

Extent of compensation for variations in monkey saccadic eye movements

Abstract. We investigated and quantified the ability of the primate saccadic system to generate accurate eye movements in spite of naturally occurring variations in saccadic speed and trajectory. We show that the amplitude of a series of saccades directed to the same target is positively correlated to their peak speed, i.e., the faster the saccade, the bigger its amplitude. We demonstrate that this result cannot be simply accounted for by the main sequence, and that on average the saccadic system is able to compensate for only 61% of the variability in speed. Deviations from the average trajectory are also only partially compensated: the underlying mechanism, which tends to bring the eyes back toward the desired trajectory, underperforms for small movements and overperforms for large movements. We also demonstrate that the performance of this compensatory mechanism, and the metrics of saccades in general, do not depend on the presence of visual information during the movement. By showing that deviations from the desired behavior are corrected during the saccade, our results further support the hypothesis that the innervation signal that generates saccadic eye movements is not pre-programmed but rather is dynamically adjusted during the movement. However, the compensation for deviations from the desired behavior is only partial, and the underlying mechanisms have yet to be completely understood. Although none of the current models of the saccadic system can account for our results, some of them, if appropriately modified, probably could.