Sensorimotor transformation elicits systematic patterns of activity along the dorsoventral extent of the superior colliculus in the macaque monkey

Massot, Corentin; Jagadisan, Uday K.; Gandhi, Neeraj J.

doi:10.1038/s42003-019-0527-y

Cited by 25 publications

(50 citation statements)

References 64 publications

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“…This layered structure, located at the roof of the brain stem, plays a critical role in transforming sensory information into eye movement commands. Population recordings have been successfully performed in the SC using linear probes [91], and it thus might be possible to identify dominant patterns of neural activity in SC using dimensionality reduction [71]. Our results predict that slow drift in the cortex should be significantly correlated with slow drift in the SC.…”

Section: Discussionmentioning

confidence: 73%

The eyes reflect an internal cognitive state hidden in the population activity of cortical neurons

Johnston

Snyder

Khanna

et al. 2020

Preprint

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SummaryDecades of research have shown that global brain states such as arousal can be indexed by measuring the properties of the eyes. Neural signals from individual neurons, populations of neurons, and field potentials measured throughout much of the brain have been associated with the size of the pupil, small fixational eye movements, and vigor in saccadic eye movements. However, precisely because the eyes have been associated with modulation of neural activity across the brain, and many different kinds of measurements of the eyes have been made across studies, it has been difficult to clearly isolate how internal states affect the behavior of the eyes, and vice versa. Recent work in our laboratory identified a latent dimension of neural activity in macaque visual cortex on the timescale of minutes to tens of minutes. This ‘slow drift’ was associated with perceptual performance on an orientation-change detection task, as well as neural activity in visual and prefrontal cortex (PFC), suggesting it might reflect a shift in a global brain state. This motivated us to ask if the neural signature of this internal state is correlated with the action of the eyes in different behavioral tasks. We recorded from visual cortex (V4) while monkeys performed a change detection task, and the prefrontal cortex, while they performed a memory-guided saccade task. On both tasks, slow drift was associated with a pattern that is indicative of changes in arousal level over time. When pupil size was large, and the subjects were in a heighted state of arousal, microsaccade rate and reaction time decreased while saccade velocity increased. These results show that the action of the eyes is associated with a dominant mode of neural activity that is pervasive and task-independent, and can be accessed in the population activity of neurons across the cortex.

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Section: Discussionmentioning

confidence: 73%

The eyes reflect an internal cognitive state hidden in the population activity of cortical neurons

Johnston

Snyder

Khanna

et al. 2020

Preprint

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“…6, 7), this notion did not hold up. Instead, all three cell populations (V, VM, M) showed similar T-G transitions, consistent with extensive sharing of information along the dorsal-ventral layers of the SC (Massot et al, 2019). It therefore appears that the reason V cells mainly coded Te was simply because (by definition) they were more active early in the transformation, whereas M cells coded G because they were mainly active later in the response.…”

Section: Spatial Coding In Different Sc Cell Types: Fixed or Dynamic?mentioning

confidence: 74%

“…Alternatively, it has been demonstrated that the SC (and other cortical gaze areas) can provide a visual-motor transformation for gaze shifts when the experimental task introduced a temporal or spatial separation between the visual stimuli and movement initiation (Gnadt and Andersen, 1988;Everling et al, 1999;Munoz and Everling, 2004;Sadeh et al, 2015;Sajad et al, 2015). Recently, the anatomic basis for this has been demonstrated at the level of SC microcircuitry, where the visual response is transmitted from dorsal to ventral layers, the delay response is similarly distributed, but motor response recruitment proceeds in the opposite direction (Massot et al, 2019).…”

Section: Evidence For a Visual To Motor Transformation In The Scmentioning

confidence: 99%

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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“…However, in that study (Hafed & Chen, 2016), we did not control for the depths of the recorded neurons from the SC surface when we analyzed the neurons’ motor bursts. Since the strength of SC motor bursts can vary substantially with depth from the SC surface (Massot et al, 2019), here, I wanted to first confirm whether the asymmetry alluded to above (Hafed & Chen, 2016) was still present when carefully controlling for neuron depth (Methods). If this was the case, I could then ask whether saccade kinematics were systematically different or not.…”

Section: Resultsmentioning

confidence: 99%

Superior colliculus saccade motor bursts do not dictate movement kinematics

Zhang

Malevich

Baumann

et al. 2021

Preprint

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The primate superior colliculus (SC) contains a topographic map of visual field locations, such that the anatomical location of any given active neuron defines a desired eye movement amplitude and direction. Complementing such a spatial code, SC neurons also exhibit saccade-related bursts that are tightly synchronized with movement onset. Current models suggest that such bursts, and their properties, constitute a temporal rate code that may dictate moment-to-moment movement evolution. However, a recent result demonstrated altered movement properties with minimal changes in SC motor burst strengths (Buonocore, Tian, Khademi, & Hafed, 2021). Here, I support such a dissociation between the SC temporal rate code and instantaneous movement evolution: SC burst strength varies depending on whether saccades are directed towards the upper or lower visual fields, but the movements themselves have similar kinematics. Thus, SC saccade-related motor bursts do not necessarily dictate movement kinematics, motivating investigating other possible functional roles for these bursts.

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Sensorimotor transformation elicits systematic patterns of activity along the dorsoventral extent of the superior colliculus in the macaque monkey

Cited by 25 publications

References 64 publications

The eyes reflect an internal cognitive state hidden in the population activity of cortical neurons

The eyes reflect an internal cognitive state hidden in the population activity of cortical neurons

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

Superior colliculus saccade motor bursts do not dictate movement kinematics

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