Pursuit-Related Neurons in the Supplementary Eye Fields: Discharge During Pursuit and Passive Whole Body Rotation

2004 ◽  
Vol 91 (6) ◽  
pp. 2809-2825 ◽  
Author(s):  
Junko Fukushima ◽  
Teppei Akao ◽  
Norihito Takeichi ◽  
Sergei Kurkin ◽  
Chris R. S. Kaneko ◽  
...  
Keyword(s):  
Smooth Pursuit ◽  
Space Velocity ◽  
Whole Body ◽  
Body Rotation ◽  
Stimulus Velocity ◽  
Chair Rotation ◽  
Vestibulo Ocular Reflex ◽  
Task Conditions ◽  
Supplementary Eye Fields ◽  
Vergence Tracking

The primate frontal cortex contains two areas related to smooth-pursuit: the frontal eye fields (FEFs) and supplementary eye fields (SEFs). To distinguish the specific role of the SEFs in pursuit, we examined discharge of a total of 89 pursuit-related neurons that showed consistent modulation when head-stabilized Japanese monkeys pursued a spot moving sinusoidally in fronto-parallel planes and/or in depth and with or without passive whole body rotation. During smooth-pursuit at different frequencies, 43% of the neurons tested (17/40) exhibited discharge amplitude of modulation linearly correlated with eye velocity. During cancellation of the vestibulo-ocular reflex and/or chair rotation in complete darkness, the majority of neurons tested (91% = 30/33) responded. However, only 17% of the responding neurons (4/30) were modulated in proportion to gaze (eye-in-space) velocity during pursuit-vestibular interactions. When the monkeys fixated a stationary spot, 20% of neurons tested (7/34) responded to motion of a second spot. Among the neurons tested for both smooth-pursuit and vergence tracking ( n = 56), 27% (15/56) discharged during both, 62% (35/56) responded during smooth-pursuit only, and 11% (6/56) during vergence tracking only. Phase shifts (relative to stimulus velocity) of responding neurons during pursuit in frontal and depth planes and during chair rotation remained virtually constant (≤1 Hz). These results, together with the robust vestibular-related discharge of most SEF neurons, show that the discharge of the majority of SEF pursuit-related neurons is quite distinct from that of caudal FEF neurons in identical task conditions, suggesting that the two areas are involved in different aspects of pursuit-vestibular interactions including predictive pursuit.

Role of the Cerebellar Flocculus Region in the Coordination of Eye and Head Movements During Gaze Pursuit

2000 ◽  
Vol 84 (3) ◽  
pp. 1614-1626 ◽  
Author(s):  
Timothy Belton ◽  
Robert A. McCrea
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Head Movements ◽  
Whole Body ◽  
Head Tracking ◽  
Smooth Pursuit Eye Movements ◽  
Body Rotation ◽  
Pursuit Eye Movements ◽  
Smooth Tracking ◽  
Eye Velocity

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive (≈43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.

Brain Stem Pursuit Pathways: Dissociating Visual, Vestibular, and Proprioceptive Inputs During Combined Eye-Head Gaze Tracking

2003 ◽  
Vol 90 (1) ◽  
pp. 271-290 ◽  
Author(s):  
Jefferson E. Roy ◽  
Kathleen E. Cullen
Keyword(s):  
Smooth Pursuit ◽  
Whole Body ◽  
Eye Position ◽  
Motor Nucleus ◽  
Body Rotation ◽  
Gaze Tracking ◽  
Primary Input ◽  
Passive Rotation ◽  
Extraocular Motoneurons ◽  
Movement Sensitivity

Eye-head (EH) neurons within the medial vestibular nuclei are thought to be the primary input to the extraocular motoneurons during smooth pursuit: they receive direct projections from the cerebellar flocculus/ventral paraflocculus, and in turn, project to the abducens motor nucleus. Here, we recorded from EH neurons during head-restrained smooth pursuit and head-unrestrained combined eye-head pursuit (gaze pursuit). During head-restrained smooth pursuit of sinusoidal and step-ramp target motion, each neuron's response was well described by a simple model that included resting discharge (bias), eye position, and velocity terms. Moreover, eye acceleration, as well as eye position, velocity, and acceleration error (error = target movement – eye movement) signals played no role in shaping neuronal discharges. During head-unrestrained gaze pursuit, EH neuron responses reflected the summation of their head-movement sensitivity during passive whole-body rotation in the dark and gaze-movement sensitivity during smooth pursuit. Indeed, EH neuron responses were well predicted by their head- and gaze-movement sensitivity during these two paradigms across conditions (e.g., combined eye-head gaze pursuit, smooth pursuit, whole-body rotation in the dark, whole-body rotation while viewing a target moving with the head (i.e., cancellation), and passive rotation of the head-on-body). Thus our results imply that vestibular inputs, but not the activation of neck proprioceptors, influence EH neuron responses during head-on-body movements. This latter proposal was confirmed by demonstrating a complete absence of modulation in the same neurons during passive rotation of the monkey's body beneath its neck. Taken together our results show that during gaze pursuit EH neurons carry vestibular- as well as gaze-related information to extraocular motoneurons. We propose that this vestibular-related modulation is offset by inputs from other premotor inputs, and that the responses of vestibuloocular reflex interneurons (i.e., position-vestibular-pause neurons) are consistent with such a proposal.

scholarly journals Galvanic stimulation of the vestibular periphery in guinea pigs during passive whole body rotation and self-generated head movement

2012 ◽  
Vol 107 (8) ◽  
pp. 2260-2270 ◽  
Author(s):  
N. Shanidze ◽  
K. Lim ◽  
J. Dye ◽  
W. M. King
Keyword(s):  
Guinea Pigs ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Galvanic Stimulation ◽  
Ocular Reflex ◽  
Anticipatory Eye Movements ◽  
Vestibulo Ocular Reflex ◽  
Vestibulospinal Neurons ◽  
Stimulation Of

Irregular vestibular afferents exhibit significant phase leads with respect to angular velocity of the head in space. This characteristic and their connectivity with vestibulospinal neurons suggest a functionally important role for these afferents in producing the vestibulo-collic reflex (VCR). A goal of these experiments was to test this hypothesis with the use of weak galvanic stimulation of the vestibular periphery (GVS) to selectively activate or suppress irregular afferents during passive whole body rotation of guinea pigs that could freely move their heads. Both inhibitory and excitatory GVS had significant effects on compensatory head movements during sinusoidal and transient whole body rotations. Unexpectedly, GVS also strongly affected the vestibulo-ocular reflex (VOR) during passive whole body rotation. The effect of GVS on the VOR was comparable in light and darkness and whether the head was restrained or unrestrained. Significantly, there was no effect of GVS on compensatory eye and head movements during volitional head motion, a confirmation of our previous study that demonstrated the extravestibular nature of anticipatory eye movements that compensate for voluntary head movements.

Purkinje Cells of the Cerebellar Dorsal Vermis: Simple-Spike Activity During Pursuit and Passive Whole-Body Rotation

2002 ◽  
Vol 87 (4) ◽  
pp. 1836-1849 ◽  
Author(s):  
Yasuhiro Shinmei ◽  
Takanobu Yamanobe ◽  
Junko Fukushima ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Spike Activity ◽  
Whole Body ◽  
Body Rotation ◽  
Head Velocity ◽  
Simple Spike ◽  
Group I ◽  
Eye Velocity ◽  
P Cells

To track a slowly moving object during whole body rotation, smooth-pursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI–VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuit-sensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR ×1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR ×1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.

Headshake Versus Whole-Body Rotation Testing of the Vestibulo-Ocular Reflex

1991 ◽  
Vol 101 (7) ◽  
pp. 695???698 ◽  
Author(s):  
Joel A. Goebel ◽  
Michael Fortin ◽  
Gary D. Paige
Keyword(s):  
Whole Body ◽  
Body Rotation ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex

Activity of Smooth Pursuit-Related Neurons in the Monkey Periarcuate Cortex During Pursuit and Passive Whole-Body Rotation

2000 ◽  
Vol 83 (1) ◽  
pp. 563-587 ◽  
Author(s):  
Kikuro Fukushima ◽  
Toshikazu Sato ◽  
Junko Fukushima ◽  
Yasuhiro Shinmei ◽  
Chris R. S. Kaneko
Keyword(s):  
Eye Movements ◽  
Opposite Direction ◽  
Smooth Pursuit ◽  
Whole Body ◽  
Visual Responses ◽  
Body Rotation ◽  
Stationary Target ◽  
Space Condition ◽  
Head Velocity ◽  
Velocity Sensitivity

Smooth pursuit and vestibularly induced eye movements interact to maintain the accuracy of eye movements in space (i.e., gaze). To understand the role played by the frontal eye fields in pursuit-vestibular interactions, we examined activity of 110 neurons in the periarcuate areas of head-stabilized Japanese monkeys during pursuit eye movements and passive whole-body rotation. The majority (92%) responded with the peak of their modulation near peak stimulus velocity during suppression of the vestibuloocular reflex (VOR) when the monkeys tracked a target that moved with the same amplitude and phase and in the same plane as the chair. We classified pursuit-related neurons ( n = 100) as gaze- velocity if their peak modulation occurred for eye (pursuit) and head (VOR suppression) movements in the same direction; the amplitude of modulation during one less than twice that of the other; and modulation was lower during target-stationary-in-space condition (VOR ×1) than during VOR suppression. In addition, we examined responses during VOR enhancement (×2) in which the target moved with equal amplitude as, but opposite direction to, the chair. Gaze-velocity neurons responded maximally for opposite directions during VOR ×2 and suppression. Based on these criteria, the majority of pursuit-related neurons (66%) were classified as gaze-velocity with preferred directions uniformly distributed. Because the majority of the remaining cells (32/34) also responded during VOR suppression, they were classified as eye/head-velocity neurons. Thirteen preferred pursuit and VOR suppression in the same direction; 13 in the opposite direction, and 6 showed biphasic modulation during VOR suppression. Eye- and gaze-velocity sensitivity of the two groups of cells were similar; mean (± SD) was 0.53 ± 0.30 and 0.50 ± 0.44 spikes/s per °/s, respectively. Gaze-velocity (but not eye/head-velocity) neurons showed significant correlation between eye- and gaze-velocity sensitivity, and both groups maintained their responses when the tracking target was extinguished briefly. The majority of pursuit-related neurons (28/43 = about 65%) responded to chair rotation in complete darkness. When the monkeys fixated a stationary target, more than half of cells tested (21/40) discharged in proportion to the velocity of retinal motion of a second laser spot (mean velocity sensitivity = 0.20 ± 0.16 spikes/s per °/s). Preferred directions of individual cells to the second spot were similar to those during pursuit. Visual responses to the second spot movement were maintained even when it was extinguished briefly. These results indicate that both retinal image- and gaze-velocity signals are carried by single periarcuate pursuit-related neurons, suggesting that these signals can provide target-velocity-in-space and gaze-velocity commands during pursuit-vestibular interactions.

Vertical Purkinje Cells of the Monkey Floccular Lobe: Simple-Spike Activity During Pursuit and Passive Whole Body Rotation

1999 ◽  
Vol 82 (2) ◽  
pp. 787-803 ◽  
Author(s):  
Kikuro Fukushima ◽  
Junko Fukushima ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Spike Activity ◽  
Whole Body ◽  
Eye Position ◽  
Body Rotation ◽  
Pursuit Eye Movements ◽  
Simple Spike ◽  
P Cells ◽  
Pitch Vor

To understand how the simian floccular lobe is involved in vertical smooth pursuit eye movements and the vertical vestibuloocular reflex (VOR), we examined simple-spike activity of 70 Purkinje (P) cells during pursuit eye movements and passive whole body rotation. Fifty-eight cells responded during vertical and 12 during horizontal pursuit. We classified P cells as vertical gaze velocity (VG˙) if their modulation occurred for movements of both the eye (during vertical pursuit) and head (during pitch VOR suppression) with the modulation during one less than twice that of the other and was less during the target-fixed-in-space condition (pitch VOR X1) than during pitch VOR suppression. VG˙ P cells constituted only a minority of vertical P cells (19%). Other vertical P cells that responded during pitch VOR suppression were classified as vertical eye and head velocity (VE˙/H˙) P cells (48%), regardless of the synergy of their response direction during smooth pursuit and VOR suppression. Vertical P cells that did not respond during pitch VOR suppression but did respond during rotation in vertical planes other than pitch were classified as off-pitch VE˙/H˙ P cells (33%). The mean eye-velocity and eye-position sensitivities of the three types of vertical P cells were similar. One-third (2/7 VG˙, 2/11 VE˙/H˙, 6/13 off-pitch VE˙/H˙), in addition, showed eye position sensitivity during saccade-free fixations. Maximal vestibular activation directions (MADs) were examined during VOR suppression by applying vertical whole body rotation with the monkeys oriented in different vertical planes. The MADs for VG˙ P cells and VE˙/H˙ P cells with eye and vestibular sensitivity in the same direction were distributed near the pitch plane, suggesting convergence of bilateral anterior canal inputs. In contrast, MADs of off-pitch VE˙/H˙ P cells and VE˙/H˙ P cells with oppositely directed eye and vestibular sensitivity were shifted toward the roll plane, suggesting convergence of anterior and posterior canal inputs of the same side. Unlike horizontal G˙ P cells, the modulation of many VG˙ and VE˙/H˙ P cells when the target was fixed in space (pitch VOR X1) was not well predicted by the linear addition of their modulations during vertical pursuit and pitch VOR suppression. These results indicate that the populations of vertical and horizontal eye-movement P cells in the floccular lobe have markedly different discharge properties and therefore may be involved in different kinds of processing of vestibular-oculomotor interactions.

scholarly journals Therapy-Resistant Atypical Downbeat Nystagmus with Vertigo Confined to Specific Head-Hanging Positions: Mapping to the Gravity Vector on a Multi-Axis Turntable

2021 ◽  
pp. 464-469
Author(s):  
Dominik Péus ◽  
Dominik Straumann ◽  
Alexander Huber ◽  
Christopher J. Bockisch ◽  
Vincent Wettstein
Keyword(s):  
Hair Cells ◽  
Whole Body ◽  
Downbeat Nystagmus ◽  
Two Dimensional ◽  
Body Rotation ◽  
Therapeutic Approaches ◽  
Atypical Case ◽  
Anterior Semicircular Canal ◽  
Head Positions ◽  
Peripheral Origin

Downbeat nystagmus (DBN) observed in head-hanging positions, may be of central or peripheral origin. Central DBN in head-hanging positions is mostly due to a disorder of the vestibulo-cerebellum, whereas peripheral DBN is usually attributed to canalolithiasis of an anterior semicircular canal. Here, we describe an atypical case of a patient who, after head trauma, experienced severe and stereotypic vertigo attacks after being placed in various head-hanging positions. Vertigo lasted 10–15 s and was always associated with a robust DBN. The provocation of transient vertigo and DBN, which both showed no decrease upon repetition of maneuvers, depended on the yaw orientation relative to the trunk and the angle of backward pitch. On a motorized, multi-axis turntable, we identified the two-dimensional Helmholtz coordinates of head positions at which vertigo and DBN occurred (<i>y</i>-axis: horizontal, space-fixed; <i>z</i>-axis: vertical, and head-fixed; <i>x</i>-axis: torsional, head-fixed, and unchanged). This two-dimensional area of DBN-associated head positions did not change when whole-body rotations took different paths (e.g., by forwarding pitch) or were executed with different velocities. Moreover, the intensity of DBN was also independent of whole-body rotation paths and velocities. So far, therapeutic approaches with repeated liberation maneuvers and cranial vibrations were not successful. We speculate that vertigo and DBN in this patient are due to macular damage, possibly an unstable otolithic membrane that, in specific orientations relative to gravity, slips into a position causing paroxysmal stimulation or inhibition of macular hair cells.

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