scholarly journals Priming of Head Premotor Circuits During Oculomotor Preparation

2007 ◽  
Vol 97 (1) ◽  
pp. 701-714 ◽  
Author(s):  
Brian D. Corneil ◽  
Douglas P. Munoz ◽  
Etienne Olivier
Keyword(s):  
Low Frequency ◽  
Neck Muscle ◽  
Target Onset ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Oculomotor Neurons ◽  
Multiple Trials ◽  
Saccade Task ◽  
Fixation Interval ◽  
Oculomotor Activity

Large, rapid gaze shifts necessitate intricate coordination of the eyes and head. Brief high-frequency bursts of activity within the intermediate and deeper layers of the superior colliculus (dSC) encode desired gaze shifts regardless of component movements of the eyes and head. However, it remains unclear whether low-frequency activity emitted by oculomotor neurons within the dSC and elsewhere has any role in eye-head gaze shifts. Here we test the hypothesis that such low-frequency activity contributes to eye-head coordination by selectively priming head premotor circuits. We exploited the capacity for short-duration (10 ms, 4 pulses) dSC stimulation to evoke neck muscle responses without compromising ocular stability, stimulating at various intervals of a “gap-saccade” task. Low-frequency neural activity in many oculomotor areas (including the dSC) is known to increase during the progression of the gap-saccade task. Stimulation was passed during either a fixation-interval while a central fixation point was illuminated, a 200-ms gap-interval between fixation point offset and target onset, or a movement-interval following target onset. In the two monkeys studied, the amplitude of evoked responses on multiple neck muscles tracked the known increases in low-frequency oculomotor activity during the gap-saccade task, being greater following stimulation passed at the end of the gap- versus the fixation-interval, and greater still when the location of stimulation during the movement interval coincided with the area of the dSC generating the ensuing saccade. In one of these monkeys, we obtained a more detailed timeline of how these results co-varied with low-frequency oculomotor activity by stimulating, across multiple trials, at different times within the fixation-, gap- and movement-intervals. Importantly, in both monkeys, baseline levels of neck EMG taken immediately prior to stimulation onset did not co-vary with the known pattern of low-frequency oculomotor activity up until the arrival of a transient burst associated with visual target onset. These baseline results demonstrate that any priming of the head premotor circuits occurs without affecting the output of neck muscle motoneurons, We conclude that low-frequency oculomotor activity primes head premotor circuits well in advance of gaze shift initiation, and in a manner distinct from its effects on the eye premotor circuits. Such distinctions presumably aid the temporal coordination of the eyes and head despite fundamentally different biomechanics.

Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges

1991 ◽  
Vol 66 (5) ◽  
pp. 1642-1666 ◽  
Author(s):  
D. P. Munoz ◽  
D. Guitton ◽  
D. Pelisson
Keyword(s):  
Discharge Rate ◽  
Low Frequency ◽  
Firing Frequency ◽  
Movement Trajectory ◽  
Visual Axis ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Movement Vector ◽  
Burst Discharge ◽  
Frequency Train

1. In this paper we describe the movement-related discharges of tectoreticular and tectoreticulospinal neurons [together called TR (S) Ns] that were recorded in the superior colliculus (SC) of alert cats trained to generate orienting movements in various behavioral situations; the cats' heads were either completely unrestrained (head free) or immobilized (head fixed). TR (S) Ns are organized into a retinotopically coded motor map. These cells can be divided into two groups, fixation TR (S) Ns [f TR (S) Ns] and orientation TR (S) Ns [oTR(S)Ns], depending on whether they are located, respectively, within or outside the zero (or area centralis) representation of the motor map in the rostral SC. 2. oTR(S)Ns discharged phasic motor bursts immediately before the onset of gaze shifts in both the head-free and head-fixed conditions. Ninety-five percent of the oTR(S)Ns tested (62/65) increased their rate of discharge before a visually triggered gaze shift, the amplitude and direction of which matched the cell's preferred movement vector. For movements along the optimal direction, each cell produced a burst discharge for gaze shifts of all amplitudes equal to or greater than the optimum. Hence, oTR(S)Ns had no distal limit to their movement fields. The timing of the burst relative to the onset of the gaze shift, however, depended on gaze shift amplitude: each TR(S)N reached its peak discharge when the instantaneous position of the visual axis relative to the target (i.e., instantaneous gaze motor error) matched the cell's optimal vector, regardless of the overall amplitude of the movement. 3. The intensity of the movement-related burst discharge depended on the behavioral context. For the same vector, the movement-related increase in firing was greatest for visually triggered movements and less pronounced when the cat oriented to a predicted target, a condition in which only 76% of the cells tested (35/46) increased their discharge rate. The weakest movement-related discharges were associated with spontaneous gaze shifts. 4. For some oTR(S)Ns, the average firing frequency in the movement-related burst was correlated to the peak velocity of the movement trajectory in both head-fixed and head-free conditions. Typically, when the head was unrestrained, the correlation to peak gaze velocity was better than that to either peak eye or head velocity alone. 5. Gaze shifts triggered by a high-frequency train of collicular microstimulation had greater peak velocities than comparable amplitude movements elicited by a low-frequency train of stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates

2015 ◽  
Vol 114 (2) ◽  
pp. 902-913 ◽  
Author(s):  
Samanthi C. Goonetilleke ◽  
Leor Katz ◽  
Daniel K. Wood ◽  
Chao Gu ◽  
Alexander C. Huk ◽  
...  
Keyword(s):  
Muscle Activity ◽  
Nonhuman Primates ◽  
Human Subjects ◽  
Neck Muscle ◽  
Visual Responses ◽  
Gaze Shifts ◽  
Head Turning ◽  
Gaze Shift ◽  
Intermediate Layers ◽  
Species Specific

Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (<100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle-specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ∼70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans.

scholarly journals Activity of long-lead burst neurons in pontine reticular formation during head-unrestrained gaze shifts

2014 ◽  
Vol 111 (2) ◽  
pp. 300-312 ◽  
Author(s):  
Mark M. G. Walton ◽  
Edward G. Freedman
Keyword(s):  
Reticular Formation ◽  
Head Movement ◽  
High Frequency ◽  
Low Frequency ◽  
Pontine Reticular Formation ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Burst Neurons ◽  
Saccade Onset ◽  
Neurophysiological Studies

Primates explore a visual scene through a succession of saccades. Much of what is known about the neural circuitry that generates these movements has come from neurophysiological studies using subjects with their heads restrained. Horizontal saccades and the horizontal components of oblique saccades are associated with high-frequency bursts of spikes in medium-lead burst neurons (MLBs) and long-lead burst neurons (LLBNs) in the paramedian pontine reticular formation. For LLBNs, the high-frequency burst is preceded by a low-frequency prelude that begins 12–150 ms before saccade onset. In terms of the lead time between the onset of prelude activity and saccade onset, the anatomical projections, and the movement field characteristics, LLBNs are a heterogeneous group of neurons. Whether this heterogeneity is endemic of multiple functional subclasses is an open question. One possibility is that some may carry signals related to head movement. We recorded from LLBNs while monkeys performed head-unrestrained gaze shifts, during which the kinematics of the eye and head components were dissociable. Many cells had peak firing rates that never exceeded 200 spikes/s for gaze shifts of any vector. The activity of these low-frequency cells often persisted beyond the end of the gaze shift and was usually related to head-movement kinematics. A subset was tested during head-unrestrained pursuit and showed clear modulation in the absence of saccades. These “low-frequency” cells were intermingled with MLBs and traditional LLBNs and may represent a separate functional class carrying signals related to head movement.

Perisaccadic Mislocalization of Visual Targets by Head-Free Gaze Shifts: Visual or Motor?

2008 ◽  
Vol 100 (4) ◽  
pp. 1848-1867 ◽  
Author(s):  
Sigrid M. C. I. van Wetter ◽  
A. John van Opstal
Keyword(s):  
Target Location ◽  
Saccadic Eye Movements ◽  
Open Loop ◽  
Spatial Updating ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Visual Probe ◽  
Saccade Onset ◽  
Saccade Direction

Such perisaccadic mislocalization is maximal in the direction of the saccade and varies systematically with the target-saccade onset delay. We have recently shown that under head-fixed conditions perisaccadic errors do not follow the quantitative predictions of current visuomotor models that explain these mislocalizations in terms of spatial updating. These models all assume sluggish eye-movement feedback and therefore predict that errors should vary systematically with the amplitude and kinematics of the intervening saccade. Instead, we reported that errors depend only weakly on the saccade amplitude. An alternative explanation for the data is that around the saccade the perceived target location undergoes a uniform transient shift in the saccade direction, but that the oculomotor feedback is, on average, accurate. This “ visual shift” hypothesis predicts that errors will also remain insensitive to kinematic variability within much larger head-free gaze shifts. Here we test this prediction by presenting a brief visual probe near the onset of gaze saccades between 40 and 70° amplitude. According to models with inaccurate gaze-motor feedback, the expected perisaccadic errors for such gaze shifts should be as large as 30° and depend heavily on the kinematics of the gaze shift. In contrast, we found that the actual peak errors were similar to those reported for much smaller saccadic eye movements, i.e., on average about 10°, and that neither gaze-shift amplitude nor kinematics plays a systematic role. Our data further corroborate the visual origin of perisaccadic mislocalization under open-loop conditions and strengthen the idea that efferent feedback signals in the gaze-control system are fast and accurate.

Visual-Vestibular Interaction Hypothesis for the Control of Orienting Gaze Shifts by Brain Stem Omnipause Neurons

2007 ◽  
Vol 97 (2) ◽  
pp. 1149-1162 ◽  
Author(s):  
Mario Prsa ◽  
Henrietta L. Galiana
Keyword(s):  
Brain Stem ◽  
Head Movements ◽  
Gaze Control ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Switching Mechanism ◽  
Interaction Hypothesis ◽  
Visual Vestibular Interaction ◽  
Motor Error ◽  
Gaze Position

Models of combined eye-head gaze shifts all aim to realistically simulate behaviorally observed movement dynamics. One of the most problematic features of such models is their inability to determine when a saccadic gaze shift should be initiated and when it should be ended. This is commonly referred to as the switching mechanism mediated by omni-directional pause neurons (OPNs) in the brain stem. Proposed switching strategies implemented in existing gaze control models all rely on a sensory error between instantaneous gaze position and the spatial target. Accordingly, gaze saccades are initiated after presentation of an eccentric visual target and subsequently terminated when an internal estimate of gaze position becomes nearly equal to that of the target. Based on behavioral observations, we demonstrate that such a switching mechanism is insufficient and is unable to explain certain types of movements. We propose an improved hypothesis for how the OPNs control gaze shifts based on a visual-vestibular interaction of signals known to be carried on anatomical projections to the OPN area. The approach is justified by the analysis of recorded gaze shifts interrupted by a head brake in animal subjects and is demonstrated by implementing the switching mechanism in an anatomically based gaze control model. Simulated performance reveals that a weighted sum of three signals: gaze motor error, head velocity, and eye velocity, hypothesized as inputs to OPNs, successfully reproduces diverse behaviorally observed eye-head movements that no other existing model can account for.

Rapid horizontal gaze movement in the monkey

1995 ◽  
Vol 73 (4) ◽  
pp. 1632-1652 ◽  
Author(s):  
J. O. Phillips ◽  
L. Ling ◽  
A. F. Fuchs ◽  
C. Siebold ◽  
J. J. Plorde
Keyword(s):  
Eye Movement ◽  
Head Movement ◽  
Vertical Axis ◽  
Head Position ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Small Correction ◽  
Horizontal Gaze

1. We studied horizontal eye and head movements in three monkeys that were trained to direct their gaze (eye position in space) toward jumping targets while their heads were both fixed and free to rotate about a vertical axis. We considered all gaze movements that traveled > or = 80% of the distance to the new visual target. 2. The relative contributions and metrics of eye and head movements to the gaze shift varied considerably from animal to animal and even within animals. Head movements could be initiated early or late and could be large or small. The eye movements of some monkeys showed a consistent decrease in velocity as the head accelerated, whereas others did not. Although all gaze shifts were hypometric, they were more hypometric in some monkeys than in others. Nevertheless, certain features of the gaze shift were identifiable in all monkeys. To identify those we analyzed gaze, eye in head position, and head position, and their velocities at three points in time during the gaze shift: 1) when the eye had completed its initial rotation toward the target, 2) when the initial gaze shift had landed, and 3) when the head movement was finished. 3. For small gaze shifts (< 20 degrees) the initial gaze movement consisted entirely of an eye movement because the head did not move. As gaze shifts became larger, the eye movement contribution saturated at approximately 30 degrees and the head movement contributed increasingly to the initial gaze movement. For the largest gaze shifts, the eye usually began counterrolling or remained stable in the orbit before gaze landed. During the interval between eye and gaze end, the head alone carried gaze to completion. Finally, when the head movement landed, it was almost aimed at the target and the eye had returned to within 10 +/- 7 degrees, mean +/- SD, of straight ahead. Between the end of the gaze shift and the end of the head movement, gaze remained stable in space or a small correction saccade occurred. 4. Gaze movements < 20 degrees landed accurately on target whether the head was fixed or free. For larger target movements, both head-free and head-fixed gaze shifts became increasingly hypometric. Head-free gaze shifts were more accurate, on average, but also more variable. This suggests that gaze is controlled in a different way with the head free. For target amplitudes < 60 degrees, head position was hypometric but the error was rather constant at approximately 10 degrees.(ABSTRACT TRUNCATED AT 400 WORDS)

Neck Muscle Responses to Stimulation of Monkey Superior Colliculus. II. Gaze Shift Initiation and Volitional Head Movements

2002 ◽  
Vol 88 (4) ◽  
pp. 2000-2018 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz
Keyword(s):  
Superior Colliculus ◽  
Neck Muscles ◽  
Head Movements ◽  
Emg Activity ◽  
Neck Muscle ◽  
Gaze Shift ◽  
Antagonist Muscles ◽  
Agonist And Antagonist ◽  
Agonist And Antagonist Muscles ◽  
Stimulation Of

We report neck muscle activity and head movements evoked by electrical stimulation of the superior colliculus (SC) in head-unrestrained monkeys. Recording neck electromyography (EMG) circumvents complications arising from the head's inertia and the kinetics of muscle force generation and allows precise assessment of the neuromuscular drive to the head plant. This study served two main purposes. First, we sought to test the predictions made in the companion paper of a parallel drive from the SC onto neck muscles. Low-current, long-duration stimulation evoked both neck EMG responses and head movements either without or prior to gaze shifts, testifying to a SC drive to neck muscles that is independent of gaze-shift initiation. However, gaze-shift initiation was linked to a transient additional EMG response and head acceleration, confirming the presence of a SC drive to neck muscles that is dependent on gaze-shift initiation. We forward a conceptual neural architecture and suggest that this parallel drive provides the oculomotor system with the flexibility to orient the eyes and head independently or together, depending on the behavioral context. Second, we compared the EMG responses evoked by SC stimulation to those that accompanied volitional head movements. We found characteristic features in the underlying pattern of evoked neck EMG that were not observed during volitional head movements in spite of the seemingly natural kinematics of evoked head movements. These features included reciprocal patterning of EMG activity on the agonist and antagonist muscles during stimulation, a poststimulation increase in the activity of antagonist muscles, and synchronously evoked responses on agonist and antagonist muscles regardless of initial horizontal head position. These results demonstrate that the electrically evoked SC drive to the head cannot be considered as a neural replicate of the SC drive during volitional head movements and place important new constraints on the interpretation of electrically evoked head movements.

scholarly journals Electrical Stimulation of the Frontal Eye Field in a Monkey Produces Combined Eye and Head Movements

2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Eye Field ◽  
A Site ◽  
Head Rotations ◽  
Stimulation Of

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.

Recruitment of a Head-Turning Synergy by Low-Frequency Activity in the Primate Superior Colliculus

2008 ◽  
Vol 100 (1) ◽  
pp. 397-411 ◽  
Author(s):  
Sam Rezvani ◽  
Brian D. Corneil
Keyword(s):  
Superior Colliculus ◽  
Low Frequency ◽  
Oculomotor System ◽  
Muscle Synergy ◽  
Emg Activity ◽  
Neck Muscle ◽  
Muscle Recruitment ◽  
Head Turning ◽  
Head Restraint ◽  
Reward Expectancy

Low-frequency activity within the oculomotor system helps bridge sensation and action. Given ocular stability, low-frequency activity sustained by some neurons within the intermediate and deep superior colliculus (dSC) is assumed to be separated from motor output. However, the dSC is an orienting structure and the influence of low-frequency dSC activity at other effectors remains untested. We studied this by simultaneously recording activity from saccade-related dSC neurons and electromyographic (EMG) activity from neck muscles that turn the head. Monkeys performed a gap-saccade paradigm with varying levels of reward expectancy. Despite head restraint and even for relatively small target eccentricities (≤10°), increasing reward expectancy for a given target increased the level of low-frequency activity on dSC neurons encoding saccades to the rewarded target and increased the recruitment of a neck muscle synergy that would turn the head toward the target. The magnitude of neck muscle recruitment correlated positively on a trial-by-trial basis with the level of low-frequency dSC activity, and such correlations were optimized when neck muscle activity was shifted about 20 ms later to account for delays in the tecto-reticulo-spinal pathway. Further, dSC activity discriminated about the side of target presentation approximately 11 ms earlier than neck EMG activity. Considered alongside neck EMG responses evoked causally by SC stimulation, our results are consistent with low-frequency dSC activity recruiting a head-turning synergy. Our results support a brain stem circuit wherein the magnitude of neck muscle recruitment reflects the difference in comparative low-frequency activation across both dSCs, perhaps because of mutually inhibitory interactions within downstream head premotor circuits.

scholarly journals Target modality determines eye-head coordination in nonhuman primates: implications for gaze control

2011 ◽  
Vol 106 (4) ◽  
pp. 2000-2011 ◽  
Author(s):  
Luis C. Populin ◽  
Abigail Z. Rajala
Keyword(s):  
Nonhuman Primates ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Midbrain Structure ◽  
The Subject ◽  
Visual Targets ◽  
Time Of Presentation

We have studied eye-head coordination in nonhuman primates with acoustic targets after finding that they are unable to make accurate saccadic eye movements to targets of this type with the head restrained. Three male macaque monkeys with experience in localizing sounds for rewards by pointing their gaze to the perceived location of sources served as subjects. Visual targets were used as controls. The experimental sessions were configured to minimize the chances that the subject would be able to predict the modality of the target as well as its location and time of presentation. The data show that eye and head movements are coordinated differently to generate gaze shifts to acoustic targets. Chiefly, the head invariably started to move before the eye and contributed more to the gaze shift. These differences were more striking for gaze shifts of <20–25° in amplitude, to which the head contributes very little or not at all when the target is visual. Thus acoustic and visual targets trigger gaze shifts with different eye-head coordination. This, coupled to the fact that anatomic evidence involves the superior colliculus as the link between auditory spatial processing and the motor system, suggests that separate signals are likely generated within this midbrain structure.

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