Decoding Target Distance and Saccade Amplitude from Population Activity in the Macaque Lateral Intraparietal Area (LIP)

Bremmer, Frank; Kaminiarz, André; Klingenhoefer, Steffen; Churan, Jan

doi:10.3389/fnint.2016.00030

Cited by 30 publications

(30 citation statements)

References 62 publications

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“…The interval widths for our fixed visual and motor windows are consistent with the literature (Wurtz and Goldberg, 1972;Sparks and Hartwich-Young, 1989;Marino et al, 2008Marino et al, , 2015DeSouza et al, 2011;Bremmer et al, 2016;Sajad et al, 2016a;Sadeh et al, 2018) and were derived from separate visual and motor responses in the memory-delay paradigm, as shown previously . The intervals used for our new spatiotemporal method (Fig.…”

Section: Spatiotemporal Analysissupporting

confidence: 80%

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

Sadeh

Sajad

Wang

et al. 2019

eNeuro

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Gaze saccades, rapid shifts of the eyes and head toward a goal, have provided fundamental insights into the neural control of movement. For example, it has been shown that the superior colliculus (SC) transforms a visual target (T) code to future gaze (G) location commands after a memory delay. However, this transformation has not been observed in "reactive" saccades made directly to a stimulus, so its contribution to normal gaze behavior is unclear. Here, we tested this using a quantitative measure of the intermediate codes between T and G, based on variable errors in gaze endpoints. We demonstrate that a rapid spatial transformation occurs within the primate's SC (Macaca mulatta) during reactive saccades, involving a shift in coding from T, through intermediate codes, to G. This spatial shift progressed continuously both across and within cell populations [visual, visuomotor (VM), motor], rather than relaying discretely between populations with fixed spatial codes. These results suggest that the SC produces a rapid, noisy, and distributed transformation that contributes to variable errors in reactive gaze shifts. Significance StatementOculomotor studies have demonstrated visuomotor (VM) transformations in structures like the superior colliculus (SC) with the use of trained behavioral manipulations, like the memory delay and anti-saccades tasks, but it is not known how this happens during normal saccades. Here, using a spatial model fitting method based on endogenous gaze errors in "reactive" gaze saccades, we show that the SC provides a rapid spatial transformation from target to gaze coding that involves visual, VM, and motor neurons. This technique demonstrates that SC spatial codes are not stable, and may provide a quantitative diagnostic marker for assessing the health of sensorimotor transformations.

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Section: Spatiotemporal Analysissupporting

confidence: 80%

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

Sadeh

Sajad

Wang

et al. 2019

eNeuro

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“…Blohm & Crawford, 2007), in the saccadic system, sensory and motor parameters are highly correlated (Freedman & Sparks, 1997; Marino et al., 2008; Smith & Crawford, 2005; Snyder, 2000). One way to overcome this challenge is to study random variations between these parameters (Bremmer, Kaminiarz, Klingenhoefer, & Churan, 2016; Keith et al., 2009; Platt & Glimcher, 1998; Wimmer, Nykamp, Constantinidis, & Compte, 2014), but neurophysiology techniques that rely on averaging often wash these out. For example, the variable scatter of gaze endpoint around target in many cases averages to zero, making it impossible to know if the activity of neurons is best described by target location or the gaze endpoint position.…”

Section: Traditional Approaches To Studying Spatial Encodingmentioning

confidence: 99%

“…The following section describes an analytic approach that was developed to test between multiple models of spatial coding in neural activity during head‐unrestrained gaze behavior. The method can be viewed as complementary to decoding approaches, where machine learning algorithms are used to derive specified information from neural data (Bremmer et al., 2016; Leavitt, Pieper, Sachs, & Martinez‐Trujillo, 2017; Glaser et al, 2017; Pruszynski & Zylberberg, 2019). The latter approach tests for implicit population codes, whereas the current method tests for explicit coding, at the level of both single units and neural populations.…”

Section: A Model‐fitting Approach Developed For Identifying Neuronalmentioning

confidence: 99%

“…(Basso & May, 2017; Bastos et al., 2012; Chandrasekaran, Peixoto, Newsome, & Shenoy, 2017; Heinzleet al, 2007; Massot, Jagadisan, & Gandhi, 2019; Sajad, Godlove, & Schall, 2019; Shin & Sommer, 2012); (b) How do the spatial codes at the individual neuron and population levels change in other visuomotor behaviors, such as express saccades (latency < 100 ms), in which the temporal visual and motor responses entirely overlap (Dorris, Pare, & Munoz, 1997; Isa, 2002)? ; (c) how does this methodology extend to other areas of the brain involved in gaze control (Bremmer et al., 2016; Schneider, Dominguez‐Vargas, Gibson, Kagan, & Wilke, 2020)?…”

Section: Theoretical Implications: a New Conceptual Model For Gaze Comentioning

confidence: 99%

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Spatiotemporal transformations for gaze control

2020

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Sensorimotor transformations require spatiotemporal coordination of signals, that is, through both time and space. For example, the gaze control system employs signals that are time‐locked to various sensorimotor events, but the spatial content of these signals is difficult to assess during ordinary gaze shifts. In this review, we describe the various models and methods that have been devised to test this question, and their limitations. We then describe a new method that can (a) simultaneously test between all of these models during natural, head‐unrestrained conditions, and (b) track the evolving spatial continuum from target (T) to future gaze coding (G, including errors) through time. We then summarize some applications of this technique, comparing spatiotemporal coding in the primate frontal eye field (FEF) and superior colliculus (SC). The results confirm that these areas preferentially encode eye‐centered, effector‐independent parameters, and show—for the first time in ordinary gaze shifts—a spatial transformation between visual and motor responses from T to G coding. We introduce a new set of spatial models (T‐G continuum) that revealed task‐dependent timing of this transformation: progressive during a memory delay between vision and action, and almost immediate without such a delay. We synthesize the results from our studies and supplement it with previous knowledge of anatomy and physiology to propose a conceptual model where cumulative transformation noise is realized as inaccuracies in gaze behavior. We conclude that the spatiotemporal transformation for gaze is both local (observed within and across neurons in a given area) and distributed (with common signals shared across remote but interconnected structures).

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“…For instance, the variability induced by memoryguided gaze shifts permitted us to discriminate target coding from the gaze coding; the initial eye and head locations allowed us to distinguish between different egocentric reference frames and variable eye and head movements for a gaze shift permitted the separation of different effectors. As opposed to the decoding methods that generally test if a spatial characteristic is implicitly coded in patterns of population activity (Bremmer et al, 2016;Brandman et al, 2017), the method employed in this study method directly examines which model best predicts the activity in spatially tuned neural responses. The logic of our response field fitting in different reference frames is schematized in Fig.…”

Section: Fitting Neural Response Fields Against Spatial Modelsmentioning

confidence: 99%

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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Decoding Target Distance and Saccade Amplitude from Population Activity in the Macaque Lateral Intraparietal Area (LIP)

Cited by 30 publications

References 62 publications

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

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

Spatiotemporal transformations for gaze control

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

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