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

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

doi:10.1111/ejn.13093

Cited by 43 publications

(98 citation statements)

References 117 publications

(206 reference statements)

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“…However, it has been suggested that saccade-related hemispheric asymmetry in PPC could be influenced by factors such as latency and dynamics (Yang and Kapoula, 2004; Vergilino-Perez et al, 2012). One thing conspicuously missing in both our Delay and Response data was contralateral selectivity in the superior colliculus (Wurtz and Albano, 1980; Munoz, 2002; Gandhi and Katnani, 2011; Sadeh et al, 2015), but this is likely related to the limitations of standard fMRI techniques in revealing subcortical activation.…”

Section: Discussionmentioning

confidence: 92%

Cortical Activation during Landmark-Centered vs. Gaze-Centered Memory of Saccade Targets in the Human: An FMRI Study

Chen

Crawford

2017

Front. Syst. Neurosci.

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A remembered saccade target could be encoded in egocentric coordinates such as gaze-centered, or relative to some external allocentric landmark that is independent of the target or gaze (landmark-centered). In comparison to egocentric mechanisms, very little is known about such a landmark-centered representation. Here, we used an event-related fMRI design to identify brain areas supporting these two types of spatial coding (i.e., landmark-centered vs. gaze-centered) for target memory during the Delay phase where only target location, not saccade direction, was specified. The paradigm included three tasks with identical display of visual stimuli but different auditory instructions: Landmark Saccade (remember target location relative to a visual landmark, independent of gaze), Control Saccade (remember original target location relative to gaze fixation, independent of the landmark), and a non-spatial control, Color Report (report target color). During the Delay phase, the Control and Landmark Saccade tasks activated overlapping areas in posterior parietal cortex (PPC) and frontal cortex as compared to the color control, but with higher activation in PPC for target coding in the Control Saccade task and higher activation in temporal and occipital cortex for target coding in Landmark Saccade task. Gaze-centered directional selectivity was observed in superior occipital gyrus and inferior occipital gyrus, whereas landmark-centered directional selectivity was observed in precuneus and midposterior intraparietal sulcus. During the Response phase after saccade direction was specified, the parietofrontal network in the left hemisphere showed higher activation for rightward than leftward saccades. Our results suggest that cortical activation for coding saccade target direction relative to a visual landmark differs from gaze-centered directional selectivity for target memory, from the mechanisms for other types of allocentric tasks, and from the directionally selective mechanisms for saccade planning and execution.

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Section: Discussionmentioning

confidence: 92%

Cortical Activation during Landmark-Centered vs. Gaze-Centered Memory of Saccade Targets in the Human: An FMRI Study

Chen

Crawford

2017

Front. Syst. Neurosci.

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“…However, they could not fully explain the observed pattern of results, as we did characterize strong eye-centered and head-centered representations in all regions and modalities, indicating that multiple reference frames were active, beyond hybrid signals. Indeed, there is consensus in the literature that eye movements or changes in eye position affect visual and auditory signals in all of the areas we tested here (Van Opstal et al, 1995;Klier et al, 2001;DeSouza et al, 2011;Lee and Groh, 2012;Sadeh et al, 2015), Sparks, 1984, 1987b, a), (Cassanello and Ferrera, 2007) (Sommer and Wurtz, 2006;. (Keith et al, 2009;Sajad et al, 2015;Sajad et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Compensating for a shifting world: evolving reference frames of visual and auditory signals across three multimodal brain areas

Caruso

Pages

Sommer

2019

Preprint

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Stimulus locations are detected differently by different sensory systems, but ultimately they yield similar percepts and behavioral responses. How the brain transcends initial differences to compute similar codes is unclear. We quantitatively compared the reference frames of two sensory modalities, vision and audition, across three interconnected brain areas involved in generating saccades, namely the frontal eye fields (FEF), lateral and medial parietal cortex (LIP/MIP), and superior colliculus (SC). We recorded from single neurons in head-restrained monkeys performing auditory-and visually-guided saccades from variable initial fixation locations, and evaluated whether their receptive fields were better described as eye-centered, head-centered, or hybrid (i.e. not anchored uniquely to head-or eye-orientation). We found a progression of reference frames across areas and across time, with considerable hybrid-ness and persistent differences between modalities during most epochs/brain regions. For both modalities, the SC was more eye-centered than the FEF, which in turn was more eye-centered than the predominantly hybrid LIP/MIP. In all three areas and temporal epochs from stimulus onset to movement, visual signals were more eye-centered than auditory signals. In the SC and FEF, auditory signals became more eye-centered at the time of the saccade than they were initially after stimulus onset, but only in the SC at the time of the saccade did the auditory signals become predominantly eye-centered. The results indicate that visual and auditory signals both undergo transformations, ultimately reaching the same final reference frame but via different dynamics across brain regions and time. SIGNIFICANCE STATEMENTModels for visual-auditory integration posit that visual signals are eye-centered throughout the brain, while auditory signals are converted from head-centered to eyecentered coordinates. We show instead that both modalities largely employ hybrid reference frames: neither fully head-nor eye-centered. In three multimodal regions involved in orienting behaviors (Intraparietal Cortex, Frontal Eye Field and Superior Colliculus) these mixed codes persist in various proportions, shifting towards eyecenteredness both across time and across brain areas. Throughout, visual signals are more eye-centered than auditory signals, until a common predominantly eye-centered code for sound finally emerges during the saccade burst in the Superior Colliculus. In summary, visual and auditory signals reach the same final reference frame but via different dynamics across brain regions and time.

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“…However, the enhancement of the visual response may reflect internal changes, e.g., greater visual attention and/or increased target salience. Although the interpretation of a flexible visual-movement continuum is based on a wealth of studies that have found little differences between visual and saccade-related responses of visuomovement neurons, it is important to mention recent studies that have shown that a systematic transformation occurs between the visual and motor responses, from representing target location in space to representing actual movement metrics (Sadeh et al, 2015;Sajad et al, 2015). Our results suggest a lack of strong functional distinction between the visual and movement bursts, but specifically with respect to initiating the movea b Figure 7.…”

Section: Discussionmentioning

confidence: 99%

Disruption of Fixation Reveals Latent Sensorimotor Processes in the Superior Colliculus

Jagadisan

Gandhi

2016

J. Neurosci.

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Executive control of voluntary movements is a hallmark of the mammalian brain. In the gaze-control network, this function is thought to be mediated by a critical balance between neurons responsible for generating movements and those responsible for fixating or suppressing movements, but the nature of this balance between the relevant elements-saccade-generating and fixation-related neuronsremains unclear. Specifically, it has been debated whether the two functions are necessarily coupled (i.e., push-and-pull) or independently controlled. Here we show that behavioral perturbation of ongoing fixation with the trigeminal blink reflex in monkeys (Macaca mulatta) alters the effective balance between fixation and saccade-generating neurons in the superior colliculus (SC) and can lead to premature gaze shifts reminiscent of compromised inhibitory control. The shift in balance is primarily driven by an increase in the activity of visuomovement neurons in the caudal SC, and the extent to which fixation-related neurons in the rostral SC play a role seems to be linked to the animal's propensity to make microsaccades. The perturbation also reveals a hitherto unknown feature of sensorimotor integration: the presence of a hidden visual response in canonical movement neurons. These findings offer new insights into the latent functional interactions, or lack thereof, between components of the gaze-control network, suggesting that the perturbation technique used here may prove to be a useful tool for probing the neural mechanisms of movement generation in executive function and dysfunction.

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

Cited by 43 publications

References 117 publications

Cortical Activation during Landmark-Centered vs. Gaze-Centered Memory of Saccade Targets in the Human: An FMRI Study

Cortical Activation during Landmark-Centered vs. Gaze-Centered Memory of Saccade Targets in the Human: An FMRI Study

Compensating for a shifting world: evolving reference frames of visual and auditory signals across three multimodal brain areas

Disruption of Fixation Reveals Latent Sensorimotor Processes in the Superior Colliculus

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