Timing Determines Tuning: A Rapid Spatial Transformation in Superior Colliculus Neurons during Reactive Gaze Shifts

Sadeh, Morteza; Sajad, Amirsaman; Wang, Hongying; Yan, Xiaogang; Crawford, J. Douglas

doi:10.1523/eneuro.0359-18.2019

Cited by 9 publications

(14 citation statements)

References 125 publications

(212 reference statements)

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“…It is thought that higher level gaze structures-lateral intraparietal cortex (LIP), frontal eye fields (FEF), superior colliculus (SC)-primarily employ eye-centered codes (Goldberg et al, 2002;Klier et al, 2001;Paré and Wurtz, 2001;Russo and Bruce, 1993;Tehovnik et al, 2000), and transform target location (T) into future gaze position (G) (Constantin et al, 2007;Everling et al, 1999;Schall et al, 1995). We recently confirmed this by fitting various spatial models against FEF and SC response field activity (Sadeh et al, 2020(Sadeh et al, , 2015Sajad et al, 2016Sajad et al, , 2015. Visual responses coded for target position in eye coordinates (Te), whereas motor responses (separated from vision by a delay) coded for future gaze position in eye coordinates (Ge), and a progressive target-to-gaze (T-G) transformation (where G includes errors relative to T) along visual-memory-motor activity.…”

Section: Introductionmentioning

confidence: 89%

Spatiotemporal Coding in the Macaque Supplementary Eye Fields: Landmark Influence in the Target-to-Gaze Transformation

Bharmauria

Sajad

Yan

et al. 2020

eNeuro

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Section: Introductionmentioning

confidence: 89%

Spatiotemporal Coding in the Macaque Supplementary Eye Fields: Landmark Influence in the Target-to-Gaze Transformation

Bharmauria

Sajad

Yan

et al. 2020

eNeuro

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“…However, this requires additional training and signals that would not be present during ordinary visually guided saccades (Munoz and Everling, 2004;Medendorp et al, 2005;Amemori and Sawaguchi, 2006), and the head was fixed in most such studies. We have extended these results to natural head-unrestrained gaze shifts in the SC and FEF Sajad et al, 2015: Sadeh et al, 2020 and here in the SEF.…”

Section: Egocentric Transformations In the Gaze Systemmentioning

confidence: 67%

“…It is also thought that these areas transform target location into future gaze plans (Schall et al, 1995;Everling et al, 1999;Constantin et al, 2007). We recently confirmed that the FEF and SC participate in a transformation from target (T) to future gaze (G) coding in eye-centered coordinates by fitting these models against response field activity during head-unrestrained gaze shifts (Sadeh et al, , 2020Sajad et al, 2015Sajad et al, , 2016.…”

Section: Introductionmentioning

confidence: 63%

Spatiotemporal coding in the macaque supplementary eye fields: landmark influence in the target-to-gaze transformation

Bharmauria

Sajad

Yan

et al. 2020

Preprint

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ABSTRACTThe supplementary eye fields (SEF) subserve high-level gaze functions and possess spatially tuned response fields, but the influence of visual landmarks on SEF response fields and their role in head-unrestrained transformations are unknown. We investigated these questions using a model-fitting approach employed recently to probe target (T) to gaze (G) and landmark-centered transformations through time in visuomotor response fields (Sajad et al., 2015; Bharmauria et al., 2020). Two head-unrestrained animals were trained to saccade toward a remembered visual target, in the presence of a visual landmark that shifted during the delay, causing gaze end points to partially shift in the same direction. 256 SEF neurons were recorded, including 68 with spatially tuned response fields. Model fits to response fields established that, like the frontal eye field (FEF) and superior colliculus (SC), spatially tuned SEF responses show a visuomotor transformation along an egocentric T-G continuum in eye-centered coordinates, with relatively poor fits to other models like T-fixed-to-landmark (T’). However, response field fits against a T-T’ continuum revealed a partial shift toward T’ in the SEF motor code, similar to the landmark influence on gaze. Unlike FEF, only motor neurons (with no visual response) showed a transient unintegrated T-T’ shift (i.e., no correlation with T-G) during the delay, and only visuomotor neurons showed an integrated shift during the final motor burst (i.e., T-T’ / T-G fits correlated). Based on these findings, we propose that frontal cortex incorporates landmark-centered information into a distributed, eyecentered target-to-gaze transformation through a reciprocal, complementary prefrontal circuit.Significance StatementIt is thought that the brain integrates egocentric (self-centered) and allocentric (landmark-centered) visual signals to generate accurate goal-directed movements, but the neural mechanism is not known. Here, by shifting a visual landmark while recording frontal cortex activity in awake behaving monkeys, we show that the supplementary eye fields (SEF) incorporates landmark-centered information (in memory and motor activity) when it transforms target location into future gaze position commands. We propose a circuit model in which the SEF provides control signals to implement an integrated gaze command in the frontal eye fields (Bharmauria et al., 2020). Taken together, these experiments explain normal ego / allocentric integration and might suggest rehabilitation strategies for neurological patients who have lost one of these visual mechanisms.

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“…Finally, using our standard methodology [13,17–21] we fit various models against these spatially tuned response fields, focusing on the intermediate reference frames between TF and TL (Fig. 3A) .…”

Section: Resultsmentioning

confidence: 99%

Landmark-Centered Coding in Frontal Cortex Visual Responses

Schütz¹,

Bharmauria²,

Yan³

et al. 2020

Preprint

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Visual landmarks influence spatial cognition, navigation and goal-directed behavior, but their influence on visual coding in sensorimotor systems is poorly understood. We hypothesized that visual responses in frontal cortex control gaze areas encode potential targets in an intermediate gaze-centered / landmark-centered reference frame that might depend on specific target-landmark configurations rather than a global mechanism. We tested this hypothesis by recording neural activity in the frontal eye fields (FEF) and supplementary eye fields (SEF) while head-unrestrained macaques engaged in a memory-delay gaze task. Visual response fields (the area of visual space where targets modulate activity) were tested for each neuron in the presence of a background landmark placed at one of four oblique configurations relative to the target stimulus. 102 of 312 FEF and 43 of 256 SEF neurons showed spatially tuned response fields in this task. We then fit these data against a mathematical continuum between a gaze-centered model and a landmark-centered model. When we pooled data across the entire dataset for each neuron, our response field fits did not deviate significantly from the gaze-centered model. However, when we fit response fields separately for each target-landmark configuration, the best fits shifted (mean 37% / 40%) toward landmark-centered coding in FEF / SEF respectively. This confirmed an intermediate gaze / landmark-centered mechanism dependent on local (configuration-dependent) interactions. Overall, these data show that external landmarks influence prefrontal visual responses, likely helping to stabilize gaze goals in the presence of variable eye and head orientations.

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Timing Determines Tuning: A Rapid Spatial Transformation in Superior Colliculus Neurons during Reactive Gaze Shifts

Cited by 9 publications

References 125 publications

Spatiotemporal Coding in the Macaque Supplementary Eye Fields: Landmark Influence in the Target-to-Gaze Transformation

Spatiotemporal Coding in the Macaque Supplementary Eye Fields: Landmark Influence in the Target-to-Gaze Transformation

Spatiotemporal coding in the macaque supplementary eye fields: landmark influence in the target-to-gaze transformation

Landmark-Centered Coding in Frontal Cortex Visual Responses

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