Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

Peel, Tyler R.; Dash, Suryadeep; Lomber, Stephen G.

doi:10.1007/s10827-020-00760-7

Cited by 15 publications

(19 citation statements)

References 54 publications

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“…Therefore, either with altered movements and minimally-altered movement commands (Buonocore et al, 2021), or with minimally-altered movements and significantly altered movement commands (this work), there is a dissociation between saccade kinematics and SC motor burst strengths. This is also consistent with evidence that saccades can have similar metrics even after altering SC activity through reversible inactivation of the frontal eye fields (Peel et al, 2020).…”

Section: Discussionsupporting

confidence: 91%

“…This, along with other evidence (e.g. (Peel, Dash, Lomber, & Corneil, 2020), motivates investigating whether saccade kinematics are indeed dictated by the SC temporal code or not. I approached this question by exploiting a large asymmetry in how the SC represents the upper versus lower visual fields in its visual sensitivity (Hafed & Chen, 2016).…”

Section: Introductionmentioning

confidence: 81%

“…This, along with other evidence (e.g. Peel, Dash, Lomber, & Corneil, 2020), motivates investigating whether saccade kinematics are indeed dictated by the SC temporal code or not.…”

Section: Introductionmentioning

confidence: 85%

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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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Section: Discussionsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 81%

See 1 more Smart Citation

Superior colliculus saccade motor bursts do not dictate movement kinematics

Zhang

Malevich

Baumann

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…The model also needs to consider other factors like input from other areas. Indeed, Peel et al, 2020 reported that the SC generates fewer saccade-related spikes during FEF inactivation, even for matched saccade amplitudes. Thus, the link between SC motor burst spiking and saccade kinematics is more loose than suggested by the model.…”

Section: Discussionmentioning

confidence: 99%

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

Buonocore

Tian

Khademi

et al. 2021

eLife

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At any moment in time, new information is sampled from the environment and interacts with ongoing brain state. Often, such interaction takes place within individual circuits that are capable of both mediating the internally ongoing plan as well as representing exogenous sensory events. Here we investigated how sensory-driven neural activity can be integrated, very often in the same neuron types, into ongoing saccade motor commands. Despite the ballistic nature of saccades, visually-induced action potentials in the rhesus macaque superior colliculus (SC), a structure known to drive eye movements, not only occurred intra-saccadically, but they were also associated with highly predictable modifications of ongoing eye movements. Such predictable modifications reflected a simultaneity of movement-related discharge at one SC site and visually-induced activity at another. Our results suggest instantaneous readout of the SC during movement generation, irrespective of activity source, and they explain a significant component of kinematic variability of motor outputs.

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“…The model also needs to consider other factors like input from other areas. Indeed, Peel et al (2019) reported that the SC generates fewer saccade-related spikes during FEF inactivation, even for matched saccade amplitudes. Thus, the link between SC spiking and saccade kinematics is more loose than suggested by the model.…”

Section: Discussionmentioning

confidence: 99%

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

Buonocore

Baumann

Hafed

2020

Preprint

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22At any moment in time, new information is sampled from the environment and interacts with 23 ongoing brain state. Often, such interaction takes place within individual circuits that are 24 capable of both mediating the internally ongoing plan as well as representing exogenous 25 sensory events. Here we investigated how sensory-driven neural activity can be integrated, 26 very often in the same neuron types, into ongoing oculomotor commands for saccades. 27Despite the ballistic nature of saccades, visually-induced action potentials in the superior 28 colliculus (SC), a structure known to drive eye movements, not only occurred intra-29 saccadically, but they were also associated with highly predictable modifications of the 30 ongoing eye movements. Such modifications were also possible by peri-saccadically 31 injecting single, double, or triple electrical microstimulation pulses into the SC. Our results 32 suggest instantaneous readout of the SC map during movement generation, irrespective of 33 activity source, and explain a significant component of kinematic variability of motor outputs. 34 35 question is important to clarify mechanisms of readout from circuits in which functional 62 multiplexing is prevalent. 63In the SC, our focus here, there have been many debates about how this structure 64 contributes to saccade control (Waitzman et al., 1991;Ivan et al., 2018). In recent proposals 65 (Goossens and Van Opstal, 2006;Van Opstal and Goossens, 2008; Goossens and Van 66 Opstal, 2012), it was suggested that every spike emitted by SC neurons during their "motor" 67 bursts contributes a mini-vector of movement tendency, such that the aggregate sum of all 68 output spikes is read out by downstream structures to result in a given movement trajectory. 69However, implicit in these models is the assumption that only action potentials within a 70 narrow time window around movement triggering (the "motor" burst) matter. Any other 71 spiking, by the same or other neurons, before or after the eye movement is irrelevant. This 72 causes a significant readout problem, since downstream neurons do not necessarily have 73 the privilege of knowing which spikes should now count for a given eye movement 74 implementation and which not. 75Indeed, from an ecological perspective, an important reason for multiplexing could be 76 exactly to maintain flexibility to rapidly react to the outside world, even in a late motor control 77 structure. In that sense, rather than invoking mechanisms that allow actively ignoring "other 78 spiking" activity outside of the currently triggered eye movement (whether spatially or 79 temporally), one would predict that SC readout, at any one moment, should be quite 80 sensitive to any spiking activity regardless of its source. We experimentally tested this 81 hypothesis. We "injected" SC spiking activity around the time of saccade generation, but at 82 a spatially dissociated location. We uncovered causal evidence that the entire landscape of 83 SC activity can instantaneously contribute to individual ...

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Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

Cited by 15 publications

References 54 publications

Superior colliculus saccade motor bursts do not dictate movement kinematics

Superior colliculus saccade motor bursts do not dictate movement kinematics

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

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