We use sequences of saccadic eye movements to continually explore our visual environments. Previous behavioral studies have established that saccades in a sequence may be programmed in parallel by the oculomotor system. In this study, we tested the neural correlates of parallel programming of saccade sequences in the frontal eye field (FEF), using single-unit electrophysiological recordings from macaques performing a sequential saccade task. It is known that FEF visual neurons instantiate target selection whereas FEF movement neurons undertake saccade preparation, where the activity corresponding to a saccade vector gradually ramps up. The question of whether FEF movement neurons are involved in concurrent processing of saccade plans is as yet unresolved. In the present study, we show that, when a peripheral target is foveated after a sequence of two saccades, presaccadic activity of FEF movement neurons for the second saccade can be activated while the first is still underway. Moreover, the onset of movement activity varied parametrically with the behaviorally measured time available for parallel programming. Although at central fixation coactivated FEF movement activity may vectorially encode the retinotopic location of the second target with respect to the fixation point or the remapped location of the second target, with respect to the first our evidence suggests the possibility of early encoding of the remapped second saccade vector. Taken together, the results indicate that movement neurons, although located terminally in the FEF visual-motor spectrum, can accomplish concurrent processing of multiple saccade plans, leading to rapid execution of saccade sequences. NEW & NOTEWORTHY The execution of purposeful sequences underlies much of goal-directed behavior. How different brain areas accomplish sequencing is poorly understood. Using a modified double-step task to generate a rapid sequence of two saccades, we demonstrate that downstream movement neurons in the frontal eye field (FEF), a prefrontal oculomotor area, allow for coactivation of the first and second movement plans that constitute the sequence. These results provide fundamental insights into the neural control of action sequencing.
The frontal eye field (FEF) is a key brain region to study visuomotor transformations because the primary input to FEF is visual in nature, whereas its output reflects the planning of behaviorally relevant saccadic eye movements. In this study, we used a memory-guided saccade task to temporally dissociate the visual epoch from the saccadic epoch through a delay epoch, and used the local field potential (LFP) along with simultaneously recorded spike data to study the visuomotor transformation process. We showed that visual latency of the LFP preceded spiking activity in the visual epoch, whereas spiking activity preceded LFP activity in the saccade epoch. We also found a spatially tuned elevation in gamma band activity (30-70 Hz), but not in the corresponding spiking activity, only during the delay epoch, whose activity predicted saccade reaction times and the cells' saccade tuning. In contrast, beta band activity (13-30 Hz) showed a nonspatially selective suppression during the saccade epoch. Taken together, these results suggest that motor plans leading to saccades may be generated internally within the FEF from local activity represented by gamma activity.T he process of generating a motor plan from visual information entails a visuomotor transformation. The frontal eye field (FEF) is one of the cortical regions that contributes to the visuomotor transformation process by participating in critical events such as target selection (1-3) and saccade preparation (4-6). In addition to FEF, other oculomotor areas such as the lateral intraparietal cortex (7), the supplementary eye fields (8), the superior colliculus (9), and the dorsolateral prefrontal cortex (10) also possess neurons with similar properties as FEF neurons. Thus, a central question that remains unresolved is to what extent do the response properties of FEF neurons represent a cause versus a consequence of computations occurring elsewhere.One approach to resolve this question of causation versus consequence, in the context of target selection, was the use of simultaneously recorded local field potentials (LFP) and spikesmaking use of the idea that the LFP represents synchronized input coming into a brain area, as opposed to spiking activity, which is thought to represent output (11)(12)(13)(14)(15). Using this approach, Monosov et al. showed that FEF received spatially nonselective input through LFP earlier than spikes in the early visual epoch; however, in the consequent target selection epoch, spiking activity of FEF neurons evolved spatial selectivity and actively discriminated between the behaviorally relevant and the irrelevant stimuli earlier than the LFP (1). Such a temporal relationship between LFP and spikes during target selection in FEF has also been studied by others using simultaneously recorded LFP and spikes, converging to the same evidence (5, 16). However, whereas these studies suggest a causal role for FEF in visual selection, the causal role of FEF in saccade preparation has not yet been reported. In this study, we asked whether sac...
Monitoring sequential information is an essential component of our daily lives. Many of these sequences are abstract, in that they do not depend on the individual stimuli, but do depend on an ordered set of rules (e.g., chop then stir when cooking). Despite the ubiquity and utility of abstract sequential monitoring, little is known about its neural mechanisms. Human rostrolateral prefrontal cortex (RLPFC) exhibits specific increases in neural activity (i.e., “ramping”) during abstract sequences. Monkey dorsolateral prefrontal cortex (DLPFC) has been shown to represent sequential information in motor (not abstract) sequence tasks, and contains a sub-region, area 46, with homologous functional connectivity to human RLPFC. To test the prediction that area 46 may represent abstract sequence information, and do so with parallel dynamics to those found in humans, we conducted functional magnetic resonance imaging (fMRI) in three male monkeys. When monkeys performed no-report abstract sequence viewing, we found that left and right area 46 responded to abstract sequential changes. Interestingly, responses to rule and number changes overlapped in right area 46 and left area 46 exhibited responses to abstract sequence rules with changes in ramping activation, similar to that observed in humans. Together, these results indicate that monkey DLPFC monitors abstract visual sequential information, potentially with a preference for different dynamics in the two hemispheres. More generally, these results show that abstract sequences are represented in functionally homologous regions across monkeys and humans.Significance StatementDaily, we complete sequences that are “abstract” because they depend on an ordered set of rules (e.g., chop then stir when cooking) rather than the identity of individual items. Little is known about how the brain tracks, or monitors, this abstract sequential information. Based on previous human work showing abstract sequence related dynamics in an analogous area, we tested if monkey dorsolateral prefrontal cortex (DLPFC), specifically area 46, represents abstract sequential information using awake monkey fMRI. We found that area 46 responded to abstract sequence changes, with a preference for more general responses on the right and dynamics similar to humans on the left. These results suggest that abstract sequences are represented in functionally homologous regions across monkeys and humans.
What are the neural correlates that distinguish goal-directed (G) from non-goal-1 directed movements (nG)? We investigated this question in the monkey frontal eye field, 2 which is implicated in voluntary control of saccades. We found that only for G-saccades, the 3 variability in spike rate across trials decreased, the regularity of spike timings within trials 4 increased, the neural activity increased earlier from baseline and had a concurrent reduction 5 of LFP beta band power. 6 7 Most movements are goal directed while others, such as fidgets, may not be. However, the 8 neural mechanism that entail these different movements is poorly studied. The macaque frontal 9 eye fields (FEF) in particular has neurons that discharge before visually guided saccades, saccades 10 made in total darkness such as learned saccades or memory-guided saccades, but not before 11 spontaneous saccades in total darkness 1 . Here we discovered that when monkeys make saccades 12 that have no obvious goal in a lit environment, FEF movement and vis-mov neurons do, in fact, 13 discharge. We asked if these seeming non-goal-directed saccades made in the light were actually 14 made to a goal that we did not discern, or if there were differences in neural activities that 15 distinguished between non-goal-directed (nG) and goal directed (G) saccades. We studied two 16 characteristics of neural response not directly visible in the firing rate but which precede 17 movements: a decrease in neural response variability 2 and a decrease in local field potential beta 18 oscillatory activity 3,4 . Previous studies have shown that decreases in response variability are 19 correlated with attention 5 , preparation of visually guided saccades 2 , the onset of a visual stimulus 6 , 20 etc; and decreases in beta power have been correlated with motor preparation, and inhibitory 21 control 7,8 among other processes 9 . Nevertheless, despite these efforts, their roles in goal-directed 22We performed all our analyses on previously published datasets of frontal eye field neurons 3,10 . 130Please refer to that study for full details. We briefly describe the experimental procedures and methods here. 132Subjects: Two adult monkeys, J (male, Macaca radiata) and G (female, Macaca mulatta) were used for 133 the experiments and were cared for in accordance with the Committee for the Purpose of Control and
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