scholarly journals Frontal eye field inactivation reduces saccade preparation in the superior colliculus, but does not alter how preparatory activity relates to saccade latency

2017 ◽  
Author(s):  
Suryadeep Dash ◽  
Tyler R. Peel ◽  
Stephen G. Lomber ◽  
Brian D. Corneil

AbstractA neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of preparatory activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of iSC preparatory activity precede shorter SRTs. The frontal eye fields (FEF) are one likely source of such iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF’s role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys we examined iSC preparatory activity during unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced fixation-related activity in the rostral iSC. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. These analyses revealed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades, suggesting that the integration of preparatory and visual signals in the SC just before saccade initiation is largely independent of the FEF for saccades generated in this task.Significance statementHow does the brain decide when to move? Here, we investigate the role of two oculomotor structures, the superior colliculus (SC) and frontal eye fields (FEF), in dictating visually-guided saccadic reaction times (SRTs). In both structures, higher levels of preparatory activity precede shorter SRTs. Here, we show that FEF inactivation increases SRTs and decreases SC preparatory activity. Surprisingly, a population-level analysis of SC preparatory activity showed a negligible impact of FEF inactivation, providing one examines SRT-matched saccades. Thus, while the FEF is one source of preparatory input to the SC, it is not a critical source, and it is not involved in the integration of preparatory activity and visual signals that precedes saccade initiation in simple visually-guided saccade tasks.

2005 ◽  
Vol 93 (1) ◽  
pp. 519-534 ◽  
Author(s):  
Masayuki Watanabe ◽  
Yasushi Kobayashi ◽  
Yuka Inoue ◽  
Tadashi Isa

To examine the role of competitive and cooperative neural interactions within the intermediate layer of superior colliculus (SC), we elevated the basal SC neuronal activity by locally injecting a cholinergic agonist nicotine and analyzed its effects on saccade performance. After microinjection, spontaneous saccades were directed toward the movement field of neurons at the injection site (affected area). For visually guided saccades, reaction times were decreased when targets were presented close to the affected area. However, when visual targets were presented remote from the affected area, reaction times were not increased regardless of the rostrocaudal level of the injection sites. The endpoints of visually guided saccades were biased toward the affected area when targets were presented close to the affected area. After this endpoint effect diminished, the trajectories of visually guided saccades remained modestly curved toward the affected area. Compared with the effects on endpoints, the effects on reaction times were more localized to the targets close to the affected area. These results are consistent with a model that saccades are triggered by the activities of neurons within a restricted region, and the endpoints and trajectories of the saccades are determined by the widespread population activity in the SC. However, because increased reaction times were not observed for saccades toward targets remote from the affected area, inhibitory interactions in the SC may not be strong enough to shape the spatial distribution of the low-frequency preparatory activities in the SC.


2018 ◽  
Vol 72 (3) ◽  
pp. 481-490 ◽  
Author(s):  
Daniel T Smith ◽  
Soazig Casteau

Salient peripheral events trigger fast, “exogenous” covert orienting. The influential premotor theory of attention argues that covert orienting of attention depends upon planned but unexecuted eye-movements. One problem with this theory is that salient peripheral events, such as offsets, appear to summon attention when used to measure covert attention (e.g., the Posner cueing task) but appear not to elicit oculomotor preparation in tasks that require overt orienting (e.g., the remote distractor paradigm). Here, we examined the effects of peripheral offsets on covert attention and saccade preparation. Experiment 1 suggested that transient offsets summoned attention in a manual detection task without triggering motor preparation planning in a saccadic localisation task, although there were a high proportion of saccadic capture errors on “no-target” trials, where a cue was presented but no target appeared. In Experiment 2, “no-target” trials were removed. Here, transient offsets produced both attentional facilitation and faster saccadic responses on valid cue trials. A third experiment showed that the permanent disappearance of an object also elicited attentional facilitation and faster saccadic reaction times. These experiments demonstrate that offsets trigger both saccade programming and covert attentional orienting, consistent with the idea that exogenous, covert orienting is tightly coupled with oculomotor activation. The finding that no-go trials attenuates oculomotor priming effects offers a way to reconcile the current findings with previous claims of a dissociation between covert attention and oculomotor control in paradigms that utilise a high proportion of catch trials.


2015 ◽  
Vol 114 (2) ◽  
pp. 1048-1058 ◽  
Author(s):  
Michele Furlan ◽  
Andrew T. Smith ◽  
Robin Walker

In recent years a small number of studies have applied functional imaging techniques to investigate visual responses in the human superior colliculus (SC), but few have investigated its oculomotor functions. Here, in two experiments, we examined activity associated with endogenous saccade preparation. We used 3-T fMRI to record the hemodynamic activity in the SC while participants were either preparing or executing saccadic eye movements. Our results showed that not only executing a saccade (as previously shown) but also preparing a saccade produced an increase in the SC hemodynamic activity. The saccade-related activity was observed in the contralateral and to a lesser extent the ipsilateral SC. A second experiment further examined the contralateral mapping of saccade-related activity with a larger range of saccade amplitudes. Increased activity was again observed in both the contralateral and ipsilateral SC that was evident for large as well as small saccades. This suggests that the ipsilateral component of the increase in BOLD is not due simply to small-amplitude saccades producing bilateral activity in the foveal fixation zone. These studies provide the first evidence of presaccadic preparatory activity in the human SC and reveal that fMRI can detect activity consistent with that of buildup neurons found in the deeper layers of the SC in studies of nonhuman primates.


2017 ◽  
Author(s):  
V. C. Caruso ◽  
D. S. Pages ◽  
M. A. Sommer ◽  
J. M. Groh

ABSTRACTWe accurately perceive the visual scene despite moving our eyes ~3 times per second, an ability that requires incorporation of eye position and retinal information. We assessed how this neural computation unfolds across three interconnected structures: frontal eye fields (FEF), intraparietal cortex (LIP/MIP), and the superior colliculus (SC). Single unit activity was assessed in head-restrained monkeys performing visually-guided saccades from different initial fixations. As previously shown, the receptive fields of most LIP/MIP neurons shifted to novel positions on the retina for each eye position, and these locations were not clearly related to each other in either eye- or head-centered coordinates (hybrid coordinates). In contrast, the receptive fields of most SC neurons were stable in eye-centered coordinates. In FEF, visual signals were intermediate between those patterns: around 60% were eye-centered, whereas the remainder showed changes in receptive field location, boundaries, or responsiveness that rendered the response patterns hybrid or occasionally head-centered. These results suggest that FEF may act as a transitional step in an evolution of coordinates between LIP/MIP and SC. The persistence across cortical areas of hybrid representations that do not provide unequivocal location labels in a consistent reference frame has implications for how these representations must be read-out.New & NoteworthyHow we perceive the world as stable using mobile retinas is poorly understood. We compared the stability of visual receptive fields across different fixation positions in three visuomotor regions. Irregular changes in receptive field position were ubiquitous in intraparietal cortex, evident but less common in the frontal eye fields, and negligible in the superior colliculus (SC), where receptive fields shifted reliably across fixations. Only the SC provides a stable labelled-line code for stimuli across saccades.


2020 ◽  
Vol 123 (5) ◽  
pp. 1907-1919 ◽  
Author(s):  
Suryadeep Dash ◽  
Tyler R. Peel ◽  
Stephen G. Lomber ◽  
Brian D. Corneil

Express saccades are the shortest-latency saccade. The frontal eye fields (FEF) are thought to promote express saccades by presetting the superior colliculus. Here, by reversibly inactivating the FEF either unilaterally or bilaterally via cortical cooling, we support this by showing that the FEF plays a facilitative but not critical role in express saccade generation. We also found that FEF inactivation lowered express saccade peak velocity, emphasizing a contribution of the FEF to express saccade kinematics.


2002 ◽  
Vol 14 (8) ◽  
pp. 1256-1263 ◽  
Author(s):  
Michael C. Dorris ◽  
Raymond M. Klein ◽  
Stefan Everling ◽  
Douglas P. Munoz

The phenomenon of inhibition of return (IOR) has generated considerable interest in cognitive neuroscience because of its putative functional role in visual search, that of placing inhibitory tags on objects that have been recently inspected so as to direct further search to novel items. Many behavioral parameters of this phenomenon have been clearly delineated, and based on indirect but converging evidence, the widely held consensus is that the midbrain superior colliculus (SC) is involved in the generation of IOR. We had previously trained monkeys on a saccadic IOR task and showed that they displayed IOR in a manner similar to that observed in humans. Here we recorded the activity of single neurons in the superficial and intermediate layers of the SC while the monkeys performed this IOR task. We found that when the target was presented at a previously cued location, the stimulus-related response was attenuated and the magnitude of this response was correlated with subsequent saccadic reaction times. Surprisingly, this observed attenuation of activity during IOR was not caused by active inhibition of these neurons because (a) they were, in fact, more active following the presentation of the cue in their response field, and (b) when we repeated the same experiment while using the saccadic response time induced by electrical micro-stimulation of the SC to judge the level of excitability of the SC circuitry during the IOR task, we found faster saccades were elicited from the cued location. Our findings demonstrate that the primate SC participates in the expression of IOR; however, the SC is not the site of the inhibition. Instead, the reduced activity in the SC reflects a signal reduction that has taken place upstream.


2016 ◽  
Vol 113 (24) ◽  
pp. 6743-6748 ◽  
Author(s):  
Nathan J. Hall ◽  
Carol L. Colby

A key structure for directing saccadic eye movements is the superior colliculus (SC). The visual pathways that project to the SC have been reported to carry only luminance information and not color information. Short-wavelength–sensitive cones (S-cones) in the retina make little or no contribution to luminance signals, leading to the conclusion that S-cone stimuli should be invisible to SC neurons. The premise that S-cone stimuli are invisible to the SC has been used in numerous clinical and human psychophysical studies. The assumption that the SC cannot use S-cone stimuli to guide behavior has never been tested. We show here that express saccades, which depend on the SC, can be driven by S-cone input. Further, express saccade reaction times and changes in SC activity depend on the amount of S-cone contrast. These results demonstrate that the SC can use S-cone stimuli to guide behavior. We conclude that the use of S-cone stimuli is insufficient to isolate SC function in psychophysical and clinical studies of human subjects.


2018 ◽  
Vol 119 (4) ◽  
pp. 1411-1421 ◽  
Author(s):  
Valeria C. Caruso ◽  
Daniel S. Pages ◽  
Marc A. Sommer ◽  
Jennifer M. Groh

We accurately perceive the visual scene despite moving our eyes ~3 times per second, an ability that requires incorporation of eye position and retinal information. In this study, we assessed how this neural computation unfolds across three interconnected structures: frontal eye fields (FEF), intraparietal cortex (LIP/MIP), and the superior colliculus (SC). Single-unit activity was assessed in head-restrained monkeys performing visually guided saccades from different initial fixations. As previously shown, the receptive fields of most LIP/MIP neurons shifted to novel positions on the retina for each eye position, and these locations were not clearly related to each other in either eye- or head-centered coordinates (defined as hybrid coordinates). In contrast, the receptive fields of most SC neurons were stable in eye-centered coordinates. In FEF, visual signals were intermediate between those patterns: around 60% were eye-centered, whereas the remainder showed changes in receptive field location, boundaries, or responsiveness that rendered the response patterns hybrid or occasionally head-centered. These results suggest that FEF may act as a transitional step in an evolution of coordinates between LIP/MIP and SC. The persistence across cortical areas of mixed representations that do not provide unequivocal location labels in a consistent reference frame has implications for how these representations must be read out. NEW & NOTEWORTHY How we perceive the world as stable using mobile retinas is poorly understood. We compared the stability of visual receptive fields across different fixation positions in three visuomotor regions. Irregular changes in receptive field position were ubiquitous in intraparietal cortex, evident but less common in the frontal eye fields, and negligible in the superior colliculus (SC), where receptive fields shifted reliably across fixations. Only the SC provides a stable labeled-line code for stimuli across saccades.


2009 ◽  
Vol 101 (6) ◽  
pp. 3199-3211 ◽  
Author(s):  
Vicente Reyes-Puerta ◽  
Roland Philipp ◽  
Werner Lindner ◽  
Lars Lünenburger ◽  
Klaus-Peter Hoffmann

Target probability has been shown to modulate motor preparatory activity of neurons in the caudal superior colliculus (SC) of the primate. Here we tested whether top-down processes, such as task predictability, influence the activity of neurons also at the rostral pole of the SC (rSC), classically related to fixation. To investigate this, double-step saccade tasks were embedded in two different paradigms, one containing unpredictable and another containing predictable tasks. During predictable tasks the animals could develop some expectation about the forthcoming second target jump, i.e., anticipate when and where to make the second saccade. Neuronal responses were recorded during both paradigms and compared, revealing the influence of task predictability on the activity of rSC neurons during specific periods of fixation. In particular, neuronal activity stayed significantly lower during the fixation period between two successive saccades in predictable than in unpredictable tasks. In addition there was a learning effect within a session during predictable conditions, i.e., the intersaccadic activity was higher in the early than in the late trials. Further, reaction times for the second saccade were shorter in predictable than in unpredictable tasks. However, we demonstrated that this difference in reaction times cannot be solely accounted for by the reported difference in neural activity, which was mainly influenced by the predictability of the tasks. With these results we show that top-down processes such as predictability are imposed on the activity of neurons in the rostral pole of the primate SC.


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