Effect of allocentric landmarks on primate gaze behavior in a cue conflict task

Li, Jirui; Sajad, Amirsaman; Marino, Robert A.; Yan, Xiaogang; Sun, Saihong; Wang, Hongying; Crawford, J. Douglas

doi:10.1167/17.5.20

Cited by 18 publications

(60 citation statements)

References 95 publications

(130 reference statements)

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“…This interpretation of the influence of a visual landmark is consistent with other studies in which the accuracy of eye or hand movements towards remembered visual targets was found to be affected by the presence of a displaced landmark (Byrne and Crawford, 2010;Camors et al, 2015;Deubel, 2004;Fiehler et al, 2014;Li et al, 2017;Schütz et al, 2013). Indeed, supporting the idea that a strong assumption for visual stability acts as a prior for landmark stability, studies in which the reliability of the visual landmark was explicitly reduced (by jittering its spatial location) demonstrated that participants' localization responses became noticeably less reliant on the landmark's location (Byrne and Crawford, 2010).…”

Section: Discussionsupporting

confidence: 91%

Visual landmarks calibrate auditory space across eye movements

Aagten-Murphy

Szinte

Taylor

et al. 2019

Preprint

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Highlights• Visual landmarks affect stimulus localization across eye movements• We show this also for auditory stimuli, even when the head remains stable • Due to a visual landmark displacement, identical auditory stimuli are perceived as shifted • This suggests that auditory space is calibrated on eye-centered maps across saccades AbstractVisual objects that are present both before and after eye movements can act as landmarks, aiding localization of other visual stimuli. We investigated whether visual landmarks would also influence auditory localization -despite participants' head position remaining unchanged. Participants made eye-movements from central fixation to a peripheral visual landmark, which either remained stationary or was covertly displaced.Following the movement, participants judged whether a stimulus (auditory or visual) was shifted in location relative to before the movement. Visual localization estimates shifted along with the landmark, although the landmark displacement itself went unnoticed. Interestingly, auditory localization estimates were also displaced.Thus, despite identical auditory input reaching the ears, two auditory stimuli originating from the same position were perceived as spatially distinct when the visual landmark moved. These results are consistent with the idea that auditory spatial information is encoded within an eye-centered reference frame and subject to spatial recalibration by visual landmarks.

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Section: Discussionsupporting

confidence: 91%

Visual landmarks calibrate auditory space across eye movements

Aagten-Murphy

Szinte

Taylor

et al. 2019

Preprint

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“…No correlation was found between the AW as a function of saccade latency (Bharmauria et al, 2020). In the behavioral investigation with the same two animals, we documented that a stable landmark leads to reduction in inaccuracy of gaze endpoints (Li et al, 2017). These results generally agree with previous cue-conflict landmark studies (Neggers et al, 2005;Byrne and Crawford, 2010;Fiehler et al, 2014) and specifically with our use of this paradigm in the same animals, with only slight differences owing to collection of data on different days (Li et al, 2017;Bharmauria et al, 2020).…”

Section: Influence Of Landmark Shift On Behaviorsupporting

confidence: 90%

“…where AW is allocentric weight; d is the projection of TG onto TT' (see below), and D is the magnitude of TT'. The AW values were mainly output between 0 and 1, where 0 refers to absolute egocentric coding and 1 stands for absolute allocentric coding, i.e., the gaze landed on T', completely following the landmark shift (Byrne and Crawford, 2010;Li et al, 2017).…”

Section: Behavioral Recordings and Analysismentioning

confidence: 99%

“…Likewise, monkeys also aim gaze to an intermediate point between conflicting ego / allocentric cues (Li et al, 2017), opening the potential for neurophysiological studies of this topic. Gaze areas, i.e., lateral intraparietal cortex (LIP), frontal eye fields (FEF), and superior colliculus (SC) primarily use eye-centered codes (Russo and Bruce, 1993;Tehovnik et al, 2000;Klier et al, 2001;Paré and Wurtz, 2001;Goldberg et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…Toward these goals, we recorded SEF neurons in two head-unrestrained monkeys while they performed gaze shifts in the presence of implicitly conflicting egocentric and allocentric cues ( Fig. 1A) (Byrne and Crawford, 2010;Li et al, 2017). We then employed our model-fitting procedure (Keith et al 2009;DeSouza et al 2011;Sajad et al 2015) to analyze the data.…”

Section: Introductionmentioning

confidence: 99%

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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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Integration of landmark and saccade target signals in macaque frontal cortex visual responses

Schütz,

Bharmauria,

Yan

et al. 2023

Commun Biol

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Visual landmarks influence spatial cognition and behavior, but their influence on visual codes for action is poorly understood. Here, we test landmark influence on the visual response to saccade targets recorded from 312 frontal and 256 supplementary eye field neurons in rhesus macaques. Visual response fields are characterized by recording neural responses to various target-landmark combinations, and then we test against several candidate spatial models. Overall, frontal/supplementary eye fields response fields preferentially code either saccade targets (40%/40%) or landmarks (30%/4.5%) in gaze fixation-centered coordinates, but most cells show multiplexed target-landmark coding within intermediate reference frames (between fixation-centered and landmark-centered). Further, these coding schemes interact: neurons with near-equal target and landmark coding show the biggest shift from fixation-centered toward landmark-centered target coding. These data show that landmark information is preserved and influences target coding in prefrontal visual responses, likely to stabilize movement goals in the presence of noisy egocentric signals.

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Effect of allocentric landmarks on primate gaze behavior in a cue conflict task

Cited by 18 publications

References 95 publications

Visual landmarks calibrate auditory space across eye movements

Visual landmarks calibrate auditory space across eye movements

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

Integration of landmark and saccade target signals in macaque frontal cortex visual responses

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