Multi-modal interface for communication operated by eye blinks, eye movements, head movements, blowing/sucking and brain waves

We used event-related fMRI to measure brain activity while subjects performed saccadic eye, head, and gaze movements to visually presented targets. Two distinct patterns of response were observed. One set of areas was equally active during eye, head, and gaze movements and consisted of the superior and inferior subdivisions of the frontal eye fields, the supplementary eye field, the intraparietal sulcus, the precuneus, area MT in the lateral occipital sulcus and subcortically in basal ganglia, thalamus, and the superior colliculus. These areas have been previously observed in functional imaging studies of human eye movements, suggesting that a common set of brain areas subserves both oculomotor and head movement control in humans, consistent with data from single-unit recording and microstimulation studies in nonhuman primates that have described overlapping eye- and head-movement representations in oculomotor control areas. A second set of areas was active during head and gaze movements but not during eye movements. This set of areas included the posterior part of the planum temporale and the cortex at the temporoparietal junction, known as the parieto-insular vestibular cortex (PIVC). Activity in PIVC has been observed during imaging studies of invasive vestibular stimulation, and we confirm its role in processing the vestibular cues accompanying natural head movements. Our findings demonstrate that fMRI can be used to study the neural basis of head movements and show that areas that control eye movements also control head movements. In addition, we provide the first evidence for brain activity associated with vestibular input produced by natural head movements as opposed to invasive caloric or galvanic vestibular stimulation.

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The vestibular-related frontal cortex and its role in smooth-pursuit eye movements and vestibular-pursuit interactions

Journal of Vestibular Research ◽

10.3233/ves-2006-161-201 ◽

2006 ◽

Vol 16 (1-2) ◽

pp. 1-22 ◽

Cited By ~ 7

Author(s):

Junko Fukushima ◽

Teppei Akao ◽

Sergei Kurkin ◽

Chris R.S. Kaneko ◽

Kikuro Fukushima

Keyword(s):

Eye Movements ◽

Frontal Cortex ◽

Smooth Pursuit ◽

Vestibular Stimulation ◽

Target Motion ◽

Head Movements ◽

Image Motion ◽

Target Velocity ◽

Eye Velocity ◽

Pursuit Neurons

In order to see clearly when a target is moving slowly, primates with high acuity foveae use smooth-pursuit and vergence eye movements. The former rotates both eyes in the same direction to track target motion in frontal planes, while the latter rotates left and right eyes in opposite directions to track target motion in depth. Together, these two systems pursue targets precisely and maintain their images on the foveae of both eyes. During head movements, both systems must interact with the vestibular system to minimize slip of the retinal images. The primate frontal cortex contains two pursuit-related areas; the caudal part of the frontal eye fields (FEF) and supplementary eye fields (SEF). Evoked potential studies have demonstrated vestibular projections to both areas and pursuit neurons in both areas respond to vestibular stimulation. The majority of FEF pursuit neurons code parameters of pursuit such as pursuit and vergence eye velocity, gaze velocity, and retinal image motion for target velocity in frontal and depth planes. Moreover, vestibular inputs contribute to the predictive pursuit responses of FEF neurons. In contrast, the majority of SEF pursuit neurons do not code pursuit metrics and many SEF neurons are reported to be active in more complex tasks. These results suggest that FEF- and SEF-pursuit neurons are involved in different aspects of vestibular-pursuit interactions and that eye velocity coding of SEF pursuit neurons is specialized for the task condition.

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Dynamics of gaze control during prey capture in freely moving mice

10.1101/2020.03.25.006817 ◽

2020 ◽

Cited By ~ 1

Author(s):

Angie M. Michaiel ◽

Elliott T.T. Abe ◽

Cristopher M. Niell

Keyword(s):

Eye Movements ◽

Visual Processing ◽

Visual Information ◽

Prey Capture ◽

Active Vision ◽

Head Movements ◽

Visual Scene ◽

Specific Point ◽

Binocular Field ◽

Freely Moving

ABSTRACTMany studies of visual processing are conducted in unnatural conditions, such as head- and gaze-fixation. As this radically limits natural exploration of the visual environment, there is much less known about how animals actively use their sensory systems to acquire visual information in natural, goal-directed contexts. Recently, prey capture has emerged as an ethologically relevant behavior that mice perform without training, and that engages vision for accurate orienting and pursuit. However, it is unclear how mice target their gaze during such natural behaviors, particularly since, in contrast to many predatory species, mice have a narrow binocular field and lack foveate vision that would entail fixing their gaze on a specific point in the visual field. Here we measured head and bilateral eye movements in freely moving mice performing prey capture. We find that the majority of eye movements are compensatory for head movements, thereby acting to stabilize the visual scene. During head turns, however, these periods of stabilization are interspersed with non-compensatory saccades that abruptly shift gaze position. Analysis of eye movements relative to the cricket position shows that the saccades do not preferentially select a specific point in the visual scene. Rather, orienting movements are driven by the head, with the eyes following in coordination to sequentially stabilize and recenter the gaze. These findings help relate eye movements in the mouse to other species, and provide a foundation for studying active vision during ethological behaviors in the mouse.

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Eye-Head Movement Coordination: Vestibulo-Ocular Reflex Suppression with Head-Fixed Target Fixation1

Journal of Vestibular Research ◽

10.3233/ves-1991-1207 ◽

1991 ◽

Vol 1 (2) ◽

pp. 161-170

Author(s):

Jean-Louis Vercher ◽

Gabriel M. Gauthier

Keyword(s):

Eye Movements ◽

Time Course ◽

Mental Arithmetic ◽

Visual Space ◽

Head Movements ◽

Total Darkness ◽

Fixed Target ◽

Ocular Reflex ◽

Optokinetic Reflex ◽

Vestibulo Ocular Reflex

To maintain clear vision, the images on the retina must remain reasonably stable. Head movements are generally dealt with successfully by counter-rotation of the eyes induced by the combined actions of the vestibulo-ocular reflex (VOR) and the optokinetic reflex. A problem of importance relates to the value of the so-called intrinsic gain of the VOR (VORG) in man, and how this gain is modulated to provide appropriate eye movements. We have studied these problems in two situations: 1. fixation of a stationary object of the visual space while the head moves; 2. fixation of an object moving with the head. These two situations were compared to a basic condition in which no visual target was allowed in order to induce “pure” VOR. Eye movements were recorded in seated subjects during stationary sinusoidal and transient rotations around the vertical axis. Subjects were in total darkness (DARK condition) and involved in mental arithmetic. Alternatively, they were provided with a small foveal target, either fixed with respect to earth (earth-fixed target: EFT condition), or moving with them (chair-fixed-target: CFT condition). The stationary rotation experiment was used as baseline for the ensuing experiment and yielded control data in agreement with the literature. In all 3 visual conditions, typical responses to transient rotations were rigorously identical during the first 200 ms. They showed, sequentially, a 16-ms delay of the eye behind the head and a rapid increase in eye velocity during 75 to 80 ms, after which the average VORG was 0.9 ± 0.15. During the following 50 to 100 ms, the gain remained around 0.9 in all three conditions. Beyond 200 ms, the VORG remained around 0.9 in DARK and increased slowly towards 1 or decreased towards zero in the EFT and CFT conditions, respectively. The time-course of the later events suggests that visual tracking mechanisms came into play to reduce retinal slip through smooth pursuit, and position error through saccades. Our data also show that in total darkness VORG is set to 0.9 in man. Lower values reported in the literature essentially reflect predictive properties of the vestibulo-ocular mechanism, particularly evident when the input signal is a sinewave.

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Contribution of the Cerebellar Flocculus to Gaze Control during Active Head Movements

Journal of Neurophysiology ◽

10.1152/jn.1999.81.6.3105 ◽

1999 ◽

Vol 81 (6) ◽

pp. 3105-3109 ◽

Cited By ~ 23

Author(s):

T. Belton ◽

R. A. McCrea

Keyword(s):

Eye Movements ◽

Cerebellar Cortex ◽

Smooth Pursuit ◽

Head Movements ◽

Gaze Control ◽

Smooth Pursuit Eye Movements ◽

Ocular Pursuit ◽

Pursuit Eye Movements ◽

Cerebellar Flocculus ◽

Visual Targets

Contribution of the cerebellar flocculus to gaze control during active head movements. The flocculus and ventral paraflocculus are adjacent regions of the cerebellar cortex that are essential for controlling smooth pursuit eye movements and for altering the performance of the vestibulo-ocular reflex (VOR). The question addressed in this study is whether these regions of the cerebellum are more globally involved in controlling gaze, regardless of whether eye or active head movements are used to pursue moving visual targets. Single-unit recordings were obtained from Purkinje (Pk) cells in the floccular region of squirrel monkeys that were trained to fixate and pursue small visual targets. Cell firing rate was recorded during smooth pursuit eye movements, cancellation of the VOR, combined eye-head pursuit, and spontaneous gaze shifts in the absence of targets. Pk cells were found to be much less sensitive to gaze velocity during combined eye–head pursuit than during ocular pursuit. They were not sensitive to gaze or head velocity during gaze saccades. Temporary inactivation of the floccular region by muscimol injection compromised ocular pursuit but had little effect on the ability of monkeys to pursue visual targets with head movements or to cancel the VOR during active head movements. Thus the signals produced by Pk cells in the floccular region are necessary for controlling smooth pursuit eye movements but not for coordinating gaze during active head movements. The results imply that individual functional modules in the cerebellar cortex are less involved in the global organization and coordination of movements than with parametric control of movements produced by a specific part of the body.

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

Journal of Neurophysiology ◽

10.1152/jn.2000.84.2.1103 ◽

2000 ◽

Vol 84 (2) ◽

pp. 1103-1106 ◽

Cited By ~ 52

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.

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

Journal of Neurophysiology ◽

10.1152/jn.2000.84.3.1614 ◽

2000 ◽

Vol 84 (3) ◽

pp. 1614-1626 ◽

Cited By ~ 32

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.

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Partial Ablations of the Flocculus and Ventral Paraflocculus in Monkeys Cause Linked Deficits in Smooth Pursuit Eye Movements and Adaptive Modification of the VOR

Journal of Neurophysiology ◽

10.1152/jn.00768.2000 ◽

2002 ◽

Vol 87 (2) ◽

pp. 912-924 ◽

Cited By ~ 139

Author(s):

H. Rambold ◽

A. Churchland ◽

Y. Selig ◽

L. Jasmin ◽

S. G. Lisberger

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Large Fraction ◽

Head Rotation ◽

Head Movements ◽

Image Motion ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Vor Adaptation ◽

Ventral Paraflocculus

The vestibuloocular reflex (VOR) generates compensatory eye movements to stabilize visual images on the retina during head movements. The amplitude of the reflex is calibrated continuously throughout life and undergoes adaptation, also called motor learning, when head movements are persistently associated with image motion. Although the floccular-complex of the cerebellum is necessary for VOR adaptation, it is not known whether this function is localized in its anterior or posterior portions, which comprise the ventral paraflocculus and flocculus, respectively. The present paper reports the effects of partial lesions of the floccular-complex in five macaque monkeys, made either surgically or with stereotaxic injection of 3-nitropropionic acid (3-NP). Before and after the lesions, smooth pursuit eye movements were tested during sinusoidal and step-ramp target motion. Cancellation of the VOR was tested by moving a target exactly with the monkey during sinusoidal head rotation. The control VOR was tested during sinusoidal head rotation in the dark and during 30°/s pulses of head velocity. VOR adaptation was studied by having the monkeys wear ×2 or ×0.25 optics for 4–7 days. In two monkeys, bilateral lesions removed all of the flocculus except for parts of folia 1 and 2 but did not produce any deficits in smooth pursuit, VOR adaptation, or VOR cancellation. We conclude that the flocculus alone probably is not necessary for either pursuit or VOR learning. In two monkeys, unilateral lesions including a large fraction of the ventral paraflocculus produced small deficits in horizontal and vertical smooth pursuit, and mild impairments of VOR adaptation and VOR cancellation. We conclude that the ventral paraflocculus contributes to both behaviors. In one monkey, a bilateral lesion of the flocculus and ventral paraflocculus produced severe deficits smooth pursuit and VOR cancellation, and a complete loss of VOR adaptation. Considering all five cases together, there was a strong correlation between the size of the deficits in VOR learning and pursuit. We found the strongest correlation between the behavior deficits and the size of the lesion of the ventral paraflocculus, a weaker but significant correlation for the full floccular complex, and no correlation with the size of the lesion of the flocculus. We conclude that 1) lesions of the floccular complex cause linked deficits in smooth pursuit and VOR adaptation, and 2) the relevant portions of the structure are primarily in the ventral paraflocculus, although the flocculus may participate.

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