Recruitment of a contralateral head turning synergy by stimulation of monkey supplementary eye fields

2012 ◽  
Vol 107 (6) ◽  
pp. 1694-1710 ◽  
Author(s):  
Brendan B. Chapman ◽  
Michael A. Pace ◽  
Sharon L. Cushing ◽  
Brian D. Corneil

The supplementary eye fields (SEF) are thought to enable higher-level aspects of oculomotor control. The goal of the present experiment was to learn more about the SEF's role in orienting, specifically by examining neck muscle recruitment evoked by stimulation of the SEF. Neck muscle activity was recorded from multiple muscles in two monkeys during SEF stimulation (100 μA, 150–300 ms, 300 Hz, with the head restrained or unrestrained) delivered 200 ms into a gap period, before a visually guided saccade initiated from a central position (doing so avoids confounds between initial position and prestimulation neck muscle activity). SEF stimulation occasionally evoked overt gaze shifts and/or head movements but almost always evoked a response that invariably consisted of a contralateral head turning synergy by increasing activity on contralateral turning muscles and decreasing activity on ipsilateral turning muscles (when background activity was present). Neck muscle responses began well in advance of evoked gaze shifts (∼30 ms after stimulation onset, leading gaze shifts by ∼40–70 ms on average), started earlier and attained a larger magnitude when accompanied by progressively larger gaze shifts, and persisted on trials without overt gaze shifts. The patterns of evoked neck muscle responses resembled those evoked by frontal eye field (FEF) stimulation, except that response latencies from the SEF were ∼10 ms longer. This basic description of the cephalomotor command evoked by SEF stimulation suggests that this structure, while further removed from the motor periphery than the FEF, accesses premotor orienting circuits in the brain stem and spinal cord in a similar manner.

2003 ◽  
Vol 89 (6) ◽  
pp. 2961-2974 ◽  
Author(s):  
Julio C. Martinez-Trujillo ◽  
Hongying Wang ◽  
J. Douglas Crawford

The supplementary eye fields (SEFs), located on the dorsomedial surface of the frontal cortex, are involved in high-level aspects of saccade generation. Some reports suggest that the same area could also be involved in the generation of motor commands for the head. If so, it is important to establish whether this structure encodes eye and head commands separately or gaze commands that give rise to coordinated eye-head movements. Here we systematically stimulated (50 μA, 300 Hz, 200 ms) the SEF of two head-free (head unrestrained) macaques while recording three-dimensional eye and head rotations. A total of 55 sites were found to consistently elicit saccade-like gaze movements, always in the contralateral direction with variable vertical components, and ranging in average amplitude from 5 to 60°. These movements were always a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between these movements and natural gaze shifts. The kinematics of the elicited movements (i.e., their temporal structure, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were indistinguishable from those of natural gaze shifts. Additionally, they obeyed the same three-dimensional constraints as natural gaze shifts (i.e., eye-in-head movements obeyed Listing's law, whereas head- and eye-in-space movements obeyed Donders' law). In summary, gaze movements evoked by stimulating the SEF were indistinguishable from natural coordinated eye-head gaze shifts. Based on this we conclude that the SEF explicitly encodes gaze and that the kinematics aspects of eye-head coordination are implicitly specified by mechanisms downstream from the SEF.


2002 ◽  
Vol 88 (4) ◽  
pp. 1980-1999 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz

The role of the primate superior colliculus (SC) in orienting head movements was studied by recording electromyographic (EMG) activity from multiple neck muscles following electrical stimulation of the SC. Combining SC stimulation with neck EMG recordings provides an objective and sensitive measure of the SC drive onto neck muscle motoneurons, particularly in relation to evoked gaze shifts. In this paper, we address how neck EMG responses to SC stimulation in head-restrained monkeys depend on the rostrocaudal, mediolateral, and dorsoventral location of the stimulating electrode within the SC and vary with manipulations of the eye position prior to stimulation onset and changes in stimulation current and duration. Stimulation predominantly evoked EMG responses on the muscles obliquus capitis inferior, rectus capitis posterior major, and splenius capitis. These responses became larger in magnitude and shorter in onset latency for progressively more caudal stimulation locations, consistent with turning the head. However, evoked responses persisted even for more rostral stimulation locations usually not associated with head movements. Manipulating initial eye position revealed that the magnitude of evoked responses became stronger as the eyes attained positions contralateral to the side of stimulation, consistent with a summation between a generic command evoked by SC stimulation and the influence of eye position on tonic neck EMG. Manipulating stimulation current and duration revealed that the relationship between gaze shifts and evoked EMG responses is not obligatory: short-duration (<20 ms) or low-current stimulation evoked neck EMG responses in the absence of gaze shifts. However, long-duration stimulation (>150 ms) occasionally revealed a transient neck EMG response aligned on the onset of sequential gaze shifts. We conclude that the SC drive to neck muscle motoneurons is far more widespread than traditionally supposed and is relayed through intervening elements which may or may not be activated in association with gaze shifts.


2015 ◽  
Vol 114 (2) ◽  
pp. 902-913 ◽  
Author(s):  
Samanthi C. Goonetilleke ◽  
Leor Katz ◽  
Daniel K. Wood ◽  
Chao Gu ◽  
Alexander C. Huk ◽  
...  

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.


2002 ◽  
Vol 88 (4) ◽  
pp. 2000-2018 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz

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.


2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating

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.


2020 ◽  
Vol 91 (1) ◽  
pp. 26-31 ◽  
Author(s):  
Roope Sovelius ◽  
Maunu Mäntylä ◽  
Heini Huhtala ◽  
Juha Oksa ◽  
Rasmus Valtonen ◽  
...  

BACKGROUND: The aim of the study was to determine the characteristics of cervical muscle activity in different head movements when using helmet mounted display in air combat maneuvering.METHODS: Cervical EMG was measured with eight F/A-18 pilots using the Joint Helmet Mounted Cueing System (JHMCS) during air combat maneuvering. In-flight Gz acceleration and continuous head position were recorded. Muscular activity was compared between head movements in isolation and combined with torso movement. In addition, the effect of the direction of head movements and the use of head support of the ejection seat on muscle activity was determined.RESULTS: Muscular loading increased in the cervical flexors and extensors when using the torso during targeting beyond the field of vision in the neutral sitting posture; the difference was significant in the flexors, but activity levels were higher in the extensors. Cervical muscles are loaded to a lesser extent if the head is kept in a stable position during Gz loading. Muscular activity in the neck muscles was higher when the pilot was moving the head out of neutral posture rather than toward neutral posture. The use of the headrest as a support decreased muscle activity in the extensors, but resulted in higher activity in the flexor muscles.DISCUSSION: All analyzed conditions were significantly affected by an increase in Gz. An increase of muscle activity with torso movements is considered as a positive factor as it reflects maintained muscular support for the cervical spine. Presented results may be helpful when specific conditioning programs and cockpit ergonomics are developed for fighter pilots.Sovelius R, Mäntylä M, Huhtala H, Oksa J, Valtonen R, Tiitola L, Leino T. Head movements and neck muscle activity during air combat maneuvering. Aerosp Med Hum Perform. 2020; 91(1):26–31.


2007 ◽  
Vol 98 (1) ◽  
pp. 360-373 ◽  
Author(s):  
Neeraj J. Gandhi ◽  
David L. Sparks

Natural movements often include actions integrated across multiple effectors. Coordinated eye-head movements are driven by a command to shift the line of sight by a desired displacement vector. Yet because extraocular and neck motoneurons are separate entities, the gaze shift command must be separated into independent signals for eye and head movement control. We report that this separation occurs, at least partially, at or before the level of pontine omnipause neurons (OPNs). Stimulation of the OPNs prior to and during gaze shifts temporally decoupled the eye and head components by inhibiting gaze and eye saccades. In contrast, head movements were consistently initiated before gaze onset, and ongoing head movements continued along their trajectories, albeit with some characteristic modulations. After stimulation offset, a gaze shift composed of an eye saccade, and a reaccelerated head movement was produced to preserve gaze accuracy. We conclude that signals subject to OPN inhibition produce the eye-movement component of a coordinated eye-head gaze shift and are not the only signals involved in the generation of the head component of the gaze shift.


2009 ◽  
Vol 101 (1) ◽  
pp. 198-206 ◽  
Author(s):  
Aarlenne Z. Khan ◽  
Gunnar Blohm ◽  
Robert M. McPeek ◽  
Philippe Lefèvre

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye–head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye–head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye–head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.


2011 ◽  
Vol 33 (11) ◽  
pp. 2155-2167 ◽  
Author(s):  
Samanthi C. Goonetilleke ◽  
Paul L. Gribble ◽  
Seyed M. Mirsattari ◽  
Timothy J. Doherty ◽  
Brian D. Corneil

1989 ◽  
Vol 147 (1) ◽  
pp. 1-20
Author(s):  
T. Teyke ◽  
K. R. Weiss ◽  
I. Kupfermann

The cerebral B cluster neurones of Aplysia californica were studied under experimental conditions designed to evoke head movements in a selective fashion: either to approach an appetitive stimulus, or to withdraw from an aversive one. Intracellular recordings indicated the presence of two types of B cluster neurones: Bn cells that had fast (narrow) spikes, and Bb cells that had slow (broad) spikes. Tactile stimulation of the tentacles, rhinophores and lips excited Bn neurones, but inhibited Bb neurones. Intracellular stimulation of Bn cells evoked contractions of body wall muscles. No contractions were observed when Bb cells were fired, indicating that it is unlikely that the Bb neurones are motor neurones. Several lines of evidence indicated that the Bn type neurones are involved in withdrawal responses but not in appetitive head turning. (1) Elimination of the descending axons of the Bn cells by lesioning the cerebropleural connectives (C-Pl connectives) did not affect the head-turning response. This lesion significantly altered the head-withdrawal response by selectively eliminating an initial fast component of the withdrawal movement. (2) In chronic recordings from the C-Pl connective, unit activity was obtained which was correlated with the presentation of an appetitive stimulus rather than with evoked or spontaneous turning movements. A substantial increase in activity also occurred during head withdrawal of the animal. On the basis of these data, we postulate that separate populations of motor neurones are responsible for the aversive withdrawal of the head, and for the directed turning response towards a stimulus.


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