A causal role for the right frontal eye fields in value comparison
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ABSTRACT:
SUBMITTER: Krajbich I
PROVIDER: S-EPMC8592572 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Microsaccades aid vision by helping to strategically sample visual scenes. Despite the importance of these small eye movements, no cortical area has ever been implicated in their generation. Here, we used unilateral and bilateral reversible inactivation of the frontal eye fields (FEF) to identify a cortical drive for microsaccades. Unexpectedly, FEF inactivation altered microsaccade metrics and kinematics. Such inactivation also impaired microsaccade deployment following peripheral cue onset, regardless of cue side or inactivation configuration. Our results demonstrate that the FEF provides critical top-down drive for microsaccade generation, particularly during the recovery of microsaccades after disruption by sensory transients. Our results constitute the first direct evidence, to our knowledge, for the contribution of any cortical area to microsaccade generation, and they provide a possible substrate for how cognitive processes can influence the strategic deployment of microsaccades.
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Project description:Learning regularities that exist in the environment can help the visual system achieve optimal efficiency while reducing computational burden. Using a pro- and anti-saccade task, studies have shown that probabilistic information regarding spatial locations can be a strong modulator of frontal eye fields (FEF) activities and consequently alter saccadic behavior. One recent study has also shown that FEF activities can be modulated by transcranial direct current stimulation, where anodal tDCS facilitated prosaccades but cathodal tDCS prolonged antisaccades. These studies together suggest that location probability and tDCS can both alter FEF activities and oculomotor performance, yet how these two modulators interact with each other remains unclear. In this study, we applied anodal or cathodal tDCS over right FEF, and participants performed an interleaved pro- and anti-saccade task. Location probability was manipulated in prosaccade trials but not antisaccade trials. We observed that anodal tDCS over rFEF facilitated prosaccdes toward low-probability locations but not to high-probability locations; whereas cathodal tDCS facilitated antisaccades away from the high-probability location (i.e., same location as the low-probability locations in prosaccades). These observed effects were specific to rFEF as tDCS over the SEF in a separate control experiment did not yield similar patterns. These effects were also more pronounced in low-performers who had slower saccade reaction time. Together, we conclude that (1) the overlapping spatial endpoint between prosaccades (i.e., toward low-probability location) and antisaccades (i.e., away from high-probability location) possibly suggest an endpoint-selective mechanism within right FEF, (2) anodal tDCS and location probability cannot be combined to produce a bigger facilitative effect, and (3) anodal rFEF tDCS works best on low-performers who had slower saccade reaction time. These observations are consistent with the homeostasis account of tDCS effect and FEF functioning.
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Project description:The nature and function of perisaccadic receptive-field (RF) remapping have been controversial. We used a delayed saccade task to reduce previous confounds and examined the remapping time course in areas LIP and FEF. In the delay period, the RF shift direction turned from the initial fixation to the saccade target. In the perisaccadic period, RFs first shifted toward the target (convergent remapping) but around the time of saccade onset/offset, the shifts became predominantly toward the post-saccadic RF locations (forward remapping). Thus, unlike forward remapping that depends on the corollary discharge (CD) of the saccade command, convergent remapping appeared to follow attention from the initial fixation to the target. We modelled the data with attention-modulated and CD-gated connections, and showed that both sets of connections emerged automatically in neural networks trained to update stimulus retinal locations across saccades. Our work thus unifies previous findings into a mechanism for transsaccadic visual stability.
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Project description:The frontal eye fields (FEFs) are core nodes of the oculomotor system contributing to saccade planning, control, and execution. Here, we aimed to reveal hemispheric asymmetries between left and right FEF in both voluntary and reflexive saccades toward horizontal and vertical targets. To this end, we applied fMRI-guided continuous theta burst stimulation (cTBS) over either left or right FEF and assessed the consequences of this disruption on saccade latencies. Using a fully counterbalanced within-subject design, we measured saccade latencies before and after the application of cTBS in eighteen healthy volunteers. In general, saccade latencies on both tasks were susceptible to our experimental manipulations, that is, voluntary saccades were slower than reflexive saccades, and downward saccades were slower than upward saccades. Contrary to our expectations, we failed to reveal any TMS-related effects on saccade latencies, and Bayesian analyses provided strong support in favor of a TMS null result for both tasks. Keeping in mind the interpretative challenges of null results, we discuss possible explanations for this absence of behavioral TMS effects, focusing on methodological differences compared to previous studies (task parameters and online vs. offline TMS interventions). We also speculate about what our results might reveal about the functional role of FEF.
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Project description:In addition to its role in shifting the line of sight, the oculomotor system is also involved in the covert orienting of visuospatial attention. Causal evidence supporting this premotor theory of attention, or oculomotor readiness hypothesis, comes from the effect of subsaccadic threshold stimulation of the oculomotor system on behavior and neural activity in the absence of evoked saccades, which parallels the effects of covert attention. Here, by recording neck-muscle activity from monkeys and systematically titrating the level of stimulation current delivered to the frontal eye fields (FEF), we show that such subsaccadic stimulation is not divorced from immediate motor output but instead evokes neck-muscle responses at latencies that approach the minimal conduction time to the motor periphery. On average, neck-muscle thresholds were approximately 25% lower than saccade thresholds, and this difference is larger for FEF sites associated with progressively larger saccades. Importantly, we commonly observed lower neck-muscle thresholds even at sites evoking saccades <or=5 degrees in magnitude, although such small saccades are not associated with head motion. Neck-muscle thresholds compare well with the current levels used in previous studies to influence behavior or neural activity through activation of FEF neurons feeding back to extrastriate cortex. Our results complement this previous work by suggesting that the neurobiologic substrate that covertly orients visuospatial attention shares this command with head premotor circuits in the brainstem, culminating with recruitment in the motor periphery.
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Project description:Voluntary allocation of visual attention is controlled by top-down signals generated within the Frontal Eye Fields (FEFs) that can change the excitability of lower-level visual areas. However, the mechanism through which this control is achieved remains elusive. Here, we emulated the generation of an attentional signal using single-pulse transcranial magnetic stimulation to activate the FEFs and tracked its consequences over the visual cortex. First, we documented changes to brain oscillations using electroencephalography and found evidence for a phase reset over occipital sites at beta frequency. We then probed for perceptual consequences of this top-down triggered phase reset and assessed its anatomical specificity. We show that FEF activation leads to cyclic modulation of visual perception and extrastriate but not primary visual cortex excitability, again at beta frequency. We conclude that top-down signals originating in FEF causally shape visual cortex activity and perception through mechanisms of oscillatory realignment.
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Project description:Shortly before saccadic eye movements, visual sensitivity at the saccade target is enhanced, at the expense of sensitivity elsewhere. Some behavioral and neural correlates of this presaccadic shift of attention resemble those of covert attention, deployed during fixation. Microstimulation in non-human primates has shown that presaccadic attention modulates perception via feedback from oculomotor to visual areas. This mechanism also seems plausible in humans, as both oculomotor and visual areas are active during saccade planning. We investigated this hypothesis by applying TMS to frontal or visual areas during saccade preparation. By simultaneously measuring perceptual performance, we show their causal and differential roles in contralateral presaccadic attention effects: Whereas rFEF+ stimulation enhanced sensitivity opposite the saccade target throughout saccade preparation, V1/V2 stimulation reduced sensitivity at the saccade target only shortly before saccade onset. These findings are consistent with presaccadic attention modulating perception through cortico-cortical feedback and further dissociate presaccadic and covert attention.
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Project description:Functional near-infrared spectroscopy (fNIRS), an imaging tool that utilizes infrared light to measure changes within the concentration of oxygenated (HbO) and deoxygenated (HbR) hemoglobin, holds promise to study functional activity from motor, visual, and memory cortical regions using stimulus-induced tasks. This study investigated the reliability for fNIRS to examine cortical activations within the frontal eye fields (FEF) while initiating vergence eye movements, the inward and outward rotation of the eyes. FNIRS data were collected from twenty participants with normal binocular vision while performing vergence eye movements compared to sustained gaze fixation within a block design during two different sessions. Reliability of the experimental protocol was assessed using the intraclass correlation coefficient (ICC). The ICC values ranged from 0.6 to 0.7 for measuring the HbO activation within the vicinity of the FEF. A frequency power spectrum analysis revealed two predominant frequencies within the functional activation signals from the FEF. One high-intensity signal was present at 0.029 Hz, centering around the block design frequency. The peak-intensity signal was observed between 0.012 and 0.018 Hz where this very low-frequency oscillation (VLFO) was hypothesized to be generated by the macrovasculature present near the FEF and should be avoided as a block design frequency in future fNIRS studies to avoid false positive results.
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Project description:The consequences of individual actions are typically unknown until well after they are executed. This fact necessitates a mechanism that bridges delays between specific actions and reward outcomes. We looked for the presence of such a mechanism in the post-movement activity of neurons in the frontal eye field (FEF), a visuomotor area in prefrontal cortex. Monkeys performed an oculomotor gamble task in which they made eye movements to different locations associated with dynamically varying reward outcomes. Behavioral data showed that monkeys tracked reward history and made choices according to their own risk preferences. Consistent with previous studies, we observed that the activity of FEF neurons is correlated with the expected reward value of different eye movements before a target appears. Moreover, we observed that the activity of FEF neurons continued to signal the direction of eye movements, the expected reward value, and their interaction well after the movements were completed and when targets were no longer within the neuronal response field. In addition, this post-movement information was also observed in local field potentials, particularly in low-frequency bands. These results show that neural signals of prior actions and expected reward value persist across delays between those actions and their experienced outcomes. These memory traces may serve a role in reward-based learning in which subjects need to learn actions predicting delayed reward.
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Project description:The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coactivated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3-9 Hz theta and a 12-30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta-band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of frontoparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands.
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