Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity

Choi, Woo Young; Guitton, Daniel

doi:10.1523/jneurosci.5038-08.2009

Cited by 31 publications

(29 citation statements)

References 47 publications

(102 reference statements)

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“…Head-restrained studies that dissociated target location from gaze kinematics by varying initial eye position (Sparks and Mays, 1980) or perturbing eye muscles have suggested that SC neurons correlate best to the former, rather than the latter. However, it has often been argued that "freeing" the head reveals a more natural spatial coding in areas like the SC (Guitton, 1992;Paré and Munoz, 2001;Klier et al, 2003;Choi and Guitton, 2009). Nevertheless, the current study also suggests that the saccade-related burst in SC activity primarily encodes visual target direction during head-unrestrained gaze shifts, despite considerable variations in eye/head kinematics.…”

Section: Target Versus Gaze Movement Codingcontrasting

confidence: 44%

“…The SC is involved in saccades and gaze control (Mays and Sparks, 1980b;Hepp et al, 1993;Tweed et al, 1998;Choi and Guitton, 2009), but it could either encode gaze kinematics (Sparks and Mays, 1980) or target information (Klier et al, 2001). Investigations of saccade dynamics during SC stimulation and recordings have suggested that the SC does influence velocity (Waitzman et al, 1991;Guitton, 1992;Van Opstal et al, 1995;Munoz et al, 1996).…”

Section: Target Versus Gaze Movement Codingmentioning

confidence: 99%

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Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

DeSouza

Keith²,

Yan³

et al. 2011

J. Neurosci.

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A sensorimotor neuron's receptive field and its frame of reference are easily conflated within the natural variability of spatial behavior. Here, we capitalized on such natural variations in 3-D eye and head positions during head-unrestrained gaze shifts to visual targets in two monkeys: to determine whether intermediate/deep layer superior colliculus (SC) receptive fields code visual targets or gaze kinematics, within four different frames of reference. Visuomotor receptive fields were either characterized during gaze shifts to visual targets from a central fixation position (32 U) or were partially characterized from each of three initial fixation points (31 U). Natural variations of initial 3-D gaze and head orientation (including torsion) provided spatial separation between four different coordinate frame models (space, head, eye, fixed-vector relative to fixation), whereas natural saccade errors provided spatial separation between target and gaze positions. Using a new statistical method based on predictive sum-of-squares, we found that in our population of 63 neurons (1) receptive field fits to target positions were significantly better than fits to actual gaze shift locations and (2) eye-centered models gave significantly better fits than the head or space frame. An intermediate frames analysis confirmed that individual neuron fits were distributed targetin-eye coordinates. Gaze position "gain" effects with the spatial tuning required for a 3-D reference frame transformation were significant in 23% (7/31) of neurons tested. We conclude that the SC primarily represents gaze targets relative to the eye but also carries early signatures of the 3-D sensorimotor transformation.

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Section: Target Versus Gaze Movement Codingcontrasting

confidence: 44%

Section: Target Versus Gaze Movement Codingmentioning

confidence: 99%

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

DeSouza

Keith²,

Yan³

et al. 2011

J. Neurosci.

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show abstract

“…Finally, gaze, eye or head commands must be defined in some frame of reference (Crawford et al ., ). Some early studies suggested that space‐fixed goals are encoded in the posterior SC (Guitton et al ., ; Roucoux et al ., ; McIlwain, ), but since then most head‐unrestrained studies (Sparks, , ; Van Opstal et al ., ; Lee & Groh, ) and head‐unrestrained studies (Freedman & Sparks, ,b; Klier et al ., ; Choi & Guitton, ; DeSouza et al ., ) have emphasized eye‐centred codes.…”

Section: Introductionmentioning

confidence: 99%

Spatial transformations between superior colliculus visual and motor response fields during head‐unrestrained gaze shifts

Sadeh

Sajad

Wang

et al. 2015

Eur J of Neuroscience

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We previously reported that visuomotor activity in the superior colliculus (SC)--a key midbrain structure for the generation of rapid eye movements--preferentially encodes target position relative to the eye (Te) during low-latency head-unrestrained gaze shifts (DeSouza et al., 2011). Here, we trained two monkeys to perform head-unrestrained gaze shifts after a variable post-stimulus delay (400-700 ms), to test whether temporally separated SC visual and motor responses show different spatial codes. Target positions, final gaze positions and various frames of reference (eye, head, and space) were dissociated through natural (untrained) trial-to-trial variations in behaviour. 3D eye and head orientations were recorded, and 2D response field data were fitted against multiple models by use of a statistical method reported previously (Keith et al., 2009). Of 60 neurons, 17 showed a visual response, 12 showed a motor response, and 31 showed both visual and motor responses. The combined visual response field population (n = 48) showed a significant preference for Te, which was also preferred in each visual subpopulation. In contrast, the motor response field population (n = 43) showed a preference for final (relative to initial) gaze position models, and the Te model was statistically eliminated in the motor-only population. There was also a significant shift of coding from the visual to motor response within visuomotor neurons. These data confirm that SC response fields are gaze-centred, and show a target-to-gaze transformation between visual and motor responses. Thus, visuomotor transformations can occur between, and even within, neurons within a single frame of reference and brain structure.

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“…Moreover, several studies have highlighted gaze shifts in which eye velocity exhibits a plateau toward the end of large gaze shifts (see, for example, Fig. 1A in Choi and Guitton 2009). Simulations by Galiana and colleagues (1992) suggest that, during the plateau phase, burst neurons continue to discharge albeit with an attenuated firing pattern; to our knowledge, electrophysiological recordings of BNs during such movements do not exist in literature.…”

Section: Template Matching and Attenuation Ratiomentioning

confidence: 99%

Matching the Oculomotor Drive During Head-Restrained and Head-Unrestrained Gaze Shifts in Monkey

Bechara

Gandhi

2010

Journal of Neurophysiology

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Bechara BP, Gandhi NJ. Matching the oculomotor drive during head-restrained and head-unrestrained gaze shifts in monkey. J Neurophysiol 104: 811-828, 2010. First published May 26, 2010 doi:10.1152/jn.01114.2009. High-frequency burst neurons in the pons provide the eye velocity command (equivalently, the primary oculomotor drive) to the abducens nucleus for generation of the horizontal component of both head-restrained (HR) and head-unrestrained (HU) gaze shifts. We sought to characterize how gaze and its eye-in-head component differ when an "identical" oculomotor drive is used to produce HR and HU movements. To address this objective, the activities of pontine burst neurons were recorded during horizontal HR and HU gaze shifts. The burst profile recorded on each HU trial was compared with the burst waveform of every HR trial obtained for the same neuron. The oculomotor drive was assumed to be comparable for the pair yielding the lowest root-mean-squared error. For matched pairs of HR and HU trials, the peak eye-in-head velocity was substantially smaller in the HU condition, and the reduction was usually greater than the peak head velocity of the HU trial. A time-varying attenuation index, defined as the difference in HR and HU eye velocity waveforms divided by head velocity [␣ ϭ (Ḣ hr Ϫ Ė hu )/Ḣ ] was computed. The index was variable at the onset of the gaze shift, but it settled at values several times greater than 1. The index then decreased gradually during the movement and stabilized at 1 around the end of gaze shift. These results imply that substantial attenuation in eye velocity occurs, at least partially, downstream of the burst neurons. We speculate on the potential roles of burst-tonic neurons in the neural integrator and various cell types in the vestibular nuclei in mediating the attenuation in eye velocity in the presence of head movements. I N T R O D U C T I O NTo align the visual axis on an object of interest, one must shift the line of sight (gaze) by rapidly moving the eyes in their orbits. For large changes in gaze, a head movement typically accompanies the eye-in-head rotation. Such rapid, coordinated movements of the eyes in the orbits and the head in space are termed head-unrestrained (HU) gaze shifts. For smaller changes in gaze or when the head is immobilized, redirections of the visual axis are executed by eye movements within the orbits. We refer to such high-velocity movements as head-restrained (HR) gaze shifts or saccades.The primary oculomotor drive that produces a saccadic rotation of the eyes in orbits is an eye velocity command from neurons in the saccadic burst generator (Robinson 1975). For horizontal eye movements, the eye velocity command is encoded as a high-frequency volley of action potentials by putative short-lead burst neurons (Van Gisbergen et al. 1981) that reside in the paramedian pontine reticular formation (PPRF) and project directly to the abducens motoneurons (Langer et al. 1986;Strassman et al. 1986a). When the head is restrained, properties of the burst specif...

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Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity

Cited by 31 publications

References 47 publications

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

Spatial transformations between superior colliculus visual and motor response fields during head‐unrestrained gaze shifts

Matching the Oculomotor Drive During Head-Restrained and Head-Unrestrained Gaze Shifts in Monkey

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