Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

Schneider, Lukas; Dominguez-Vargas, Adan-Ulises; Gibson, Lydia; Kagan, Igor; Wilke, Melanie

doi:10.1101/681130

Cited by 4 publications

(8 citation statements)

References 131 publications

(237 reference statements)

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“…Since the SC does not project directly to ACC, the LP may serve as one of the feedback pathways for ACC‐SC circuits. Multiple human and nonhuman primate studies implicate the pulvinar, SC, FEFs, and ACC together in attentional orienting (Rafal & Posner, 1987) and oculomotor functions (Schneider et al., 2020). Together with the abundance of pretectal inputs to LP→ACC neurons, it is likely that intermediate and deep layer SC inputs to medial LP in rodents are also involved in visuomotor orienting.…”

Section: Discussionmentioning

confidence: 99%

Brain‐wide mapping of inputs to the mouse lateral posterior (LP/Pulvinar) thalamus–anterior cingulate cortex network

Leow

Zhou

Sullivan

et al. 2022

J of Comparative Neurology

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The rodent homolog of the primate pulvinar, the lateral posterior (LP) thalamus, is extensively interconnected with multiple cortical areas. While these cortical interactions can span the entire LP, subdivisions of the LP are characterized by differential connections with specific cortical regions. In particular, the medial LP has reciprocal connections with frontoparietal cortical areas, including the anterior cingulate cortex (ACC). The ACC plays an integral role in top-down sensory processing and attentional regulation, likely exerting some of these functions via the LP. However, little is known about how ACC and LP interact, and about the information potentially integrated in this reciprocal network. Here, we address this gap by employing a projectionspecific monosynaptic rabies tracing strategy to delineate brain-wide inputs to bottomup LP→ACC and top-down ACC→LP neurons. We find that LP→ACC neurons receive inputs from widespread cortical regions, including primary and higher order sensory and motor cortical areas. LP→ACC neurons also receive extensive subcortical inputs, particularly from the intermediate and deep layers of the superior colliculus (SC).Sensory inputs to ACC→LP neurons largely arise from visual cortical areas. In addition, ACC→LP neurons integrate cross-hemispheric prefrontal cortex inputs as well as inputs from higher order medial cortex. Our brain-wide anatomical mapping of inputs to the reciprocal LP-ACC pathways provides a roadmap for understanding how LP and ACC communicate different sources of information to mediate attentional control and visuomotor functions.

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Section: Discussionmentioning

confidence: 99%

Brain‐wide mapping of inputs to the mouse lateral posterior (LP/Pulvinar) thalamus–anterior cingulate cortex network

Leow

Zhou

Sullivan

et al. 2022

J of Comparative Neurology

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“…(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%

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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“…The notable exception is a study that covered both lateral and medial parts of the dorsal pulvinar, predominantly at the border between the two (Benevento and Port 1995). Our recording sites were largely within the medial pulvinar (MPul) or around the border between the medial and the lateral pulvinar (see also (Dominguez-Vargas et al 2017; Schneider et al 2019)). We did not observe any clear patterns along the dorsal/lateral – ventral/medial axis in the features we tested, and such patterns have also not been reported in the previous work.…”

Section: Discussionmentioning

confidence: 99%

“…Beyond the question of target selection in the memory-guided oculomotor task, dPul might be more involved in guiding other movements such as hand actions, as suggested by the effect of pulvinar inactivation or lesions on target selection via reaching and grasping, and hand-specific deficits (Wilke, Turchi, et al 2010; Wilke et al 2018). Furthermore, given that a considerable amount of dPul units showed gain-field like properties or other types of postural modulations by the position of the eyes in the orbit (Schneider et al 2019), it remains important to assess if pulvinar is causally involved in spatial reference frame transformations and eye-hand coordination.…”

Section: Discussionmentioning

confidence: 99%

“…The authors suggested that only when the stimulus serves as an immediate saccade target the visual response takes place, although it is not the pattern typically observed in the frontoparietal cortical areas. Finally, we recently have shown that dPul neurons carry information about static eye position and combine spatial encoding in eye-centered and nonretinocentric coordinates, potentially contributing to coordinate frame transformations (Schneider et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Visual, delay and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

Schneider

Dominguez-Vargas

Gibson

et al. 2021

Preprint

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Causal perturbation studies suggest that the primate dorsal pulvinar (dPul) plays a crucial role in target selection and saccade planning, but many of its basic visuomotor neuronal properties are unclear. While some functional aspects of dPul and interconnected frontoparietal areas - such as ipsilesional choice bias after inactivation - are similar, it is not known if dPul neurons share oculomotor response properties of cortical circuitry. In particular, the delay period and choice-related activity have not been explored. Here we investigated visuomotor timing and tuning in macaque dPul during instructed and free choice memory saccades using electrophysiological recordings. Most units (80%) showed significant visual (16%), visuomotor (29%) or motor-related (35%) responses. Visual cue responses were mainly contralaterally-tuned; motor responses showed weak contralateral bias. Saccade-related responses (enhancement and suppression) were more common (64%) than cue-driven responses (45%). Pre-saccadic enhancement was less frequent (9-15% depending on the definition), and only few units exhibited classical visuomotor patterns such as a combination of cue and continuous delay period activity up to the saccade onset, or pre-saccadic ramping. Instead, activity was often suppressed during movement planning (30%) and execution phases (19%). Interestingly, most spatially-selective neurons did not encode the upcoming decision during the delay in free choice trials. Thus, in absence of a visible goal, the dorsal pulvinar has only a limited role in the prospective motor planning, with response patterns partially complementary to its frontoparietal cortical partners. Conversely, prevalent cue and post-saccadic responses imply that the dorsal pulvinar participates in integrating spatial goals with processing across saccades.

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Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

Cited by 4 publications

References 131 publications

Brain‐wide mapping of inputs to the mouse lateral posterior (LP/Pulvinar) thalamus–anterior cingulate cortex network

Brain‐wide mapping of inputs to the mouse lateral posterior (LP/Pulvinar) thalamus–anterior cingulate cortex network

Spatiotemporal transformations for gaze control

Visual, delay and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

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