Dissociation of response variability from firing rate effects in frontal eye field neurons during visual stimulation, working memory, and attention.

Recent studies suggest that trial-to-trial variability of neuronal spiking responses may provide important information about behavioral state. Observed changes in variability during sensory stimulation, attention, motor preparation, and visual discrimination suggest that variability may reflect the engagement of neurons in a behavioral task. We examined changes in spiking variability of frontal eye field (FEF) neurons in a change detection task requiring monkeys to remember a visually cued location and direct attention to that location while ignoring distracters elsewhere. In this task, the firing rates (FRs) of FEF neurons not only continuously reflect the location of the remembered cue and select targets, but also predict detection performance on a trial-by-trial basis. Changes in FEF response variability, as measured by the Fano factor (FF), showed clear dissociations from changes in FR. The FF declined in response to visual stimulation at all tested locations, even in the opposite hemifield, indicating much broader spatial tuning of the FF compared with the FR. Furthermore, despite robust spatial modulation of the FR throughout all epochs of the task, spatial tuning of the FF did not persist throughout the delay period, nor did it show attentional modulation. These results indicate that changes in variability, at least in the FEF, are most effectively driven by visual stimulation, while behavioral engagement is not sufficient. Instead, changes in variability may reflect shifts in the balance between feedforward and recurrent sources of excitatory drive.

Selection and maintenance of spatial information by frontal eye field neurons.

Voluntary attention is often allocated according to internally maintained goals. Recent evidence indicates that the frontal eye field (FEF) participates in the deployment of spatial attention, even in the absence of saccadic eye movements. In addition, many FEF neurons maintain persistent representations of impending saccades. However, the role of persistent activity in the general maintenance of spatial information, and its relationship to spatial attention, has not been explored. We recorded the responses of single FEF neurons in monkeys trained to remember cued locations in order to detect changes in targets embedded among distracters in a task that did not involve saccades. We found that FEF neurons persistently encoded the cued location throughout the trial during the delay period, when no visual stimuli were present, and during visual discrimination. Furthermore, FEF activity reliably predicted whether monkeys would detect the target change. Population analyses revealed that FEF neurons with persistent activity were more effective at selecting the target from among distracters than neurons lacking persistent activity. These results demonstrate that FEF neurons maintain spatial information in the absence of saccade preparation and suggest that this maintenance contributes to the selection of relevant visual stimuli.

Top-down control of visual attention.

Top-down visual attention improves perception of selected stimuli and that improvement is reflected in the neural activity at many stages throughout the visual system. Recent studies of top-down attention have elaborated on the signatures of its effects within visual cortex and have begun identifying its causal basis. Evidence from these studies suggests that the correlates of spatial attention exhibited by neurons within the visual system originate from a distributed network of structures involved in the programming of saccadic eye movements. We summarize this evidence and discuss its relationship to the neural mechanisms of spatial working memory.

Presaccadic discrimination of receptive field stimuli by area V4 neurons.

Previous studies have shown that the visual responses of neurons in extrastriate area V4 are enhanced prior to saccadic eye movements that target receptive field (RF) stimuli. We used receiver-operator characteristic (ROC) analysis to quantify how well V4 neurons could discriminate stable RF stimuli targeted by visually-guided saccades or ignored during saccades elsewhere. We found that discrimination was transiently enhanced prior to saccades to RF stimuli whereas it was reduced prior to saccades elsewhere. Similar to what is observed during covert attention and after frontal eye field microstimulation, the changes in stimulus discrimination were due in part to changes in response magnitude. In addition, we found evidence of an increased reliability of responses when saccades were made to the RF stimulus. These results highlight the similarity of mechanisms driving covert spatial attention and the preparation of visually-guided saccades.