Kirk G. Thompson

A visual salience map in the primate frontal eye field

Models of attention and saccade target selection propose that within the brain there is a topographic map of visual salience that combines bottom-up and top-down influences to identify locations for further processing. The results of a series of experiments with monkeys performing visual search tasks have identified a population of frontal eye field (FEF) visually responsive neurons that exhibit all of the characteristics of a visual salience map. The activity of these FEF neurons is not sensitive to specific features of visual stimuli; but instead, their activity evolves over time to select the target of the search array. This selective activation reflects both the bottom-up intrinsic conspicuousness of the stimuli and the top-down knowledge and goals of the viewer. The peak response within FEF specifies the target for the overt gaze shift. However, the selective activity in FEF is not in itself a motor command because the magnitude of activation reflects the relative behavioral significance of the different stimuli in the visual scene and occurs even when no saccade is made. Identifying a visual salience map in FEF validates the theoretical concept of a salience map in many models of attention. In addition, it strengthens the emerging view that FEF is not only involved in producing overt gaze shifts, but is also important for directing covert spatial attention.

Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field

The influential “premotor theory of attention” proposes that developing oculomotor commands mediate covert visual spatial attention. A likely source of this attentional bias is the frontal eye field (FEF), an area of the frontal cortex involved in converting visual information into saccade commands. We investigated the link between FEF activity and covert spatial attention by recording from FEF visual and saccade-related neurons in monkeys performing covert visual search tasks without eye movements. Here we show that the source of attention signals in the FEF is enhanced activity of visually responsive neurons. At the time attention is allocated to the visual search target, nonvisually responsive saccade-related movement neurons are inhibited. Therefore, in the FEF, spatial attention signals are independent of explicit saccade command signals. We propose that spatially selective activity in FEF visually responsive neurons corresponds to the mental spotlight of attention via modulation of ongoing visual processing.

Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis

The purpose of this study was to investigate the temporal relationship between presaccadic neuronal discharges in the frontal eye fields (FEF) and supplementary eye fields (SEF) and the initiation of saccadic eye movements in macaque. We utilized an analytical technique that could reliably identify periods of neuronal modulation in individual spike trains. By comparing the observed activity of neurons with the random Poisson distribution generated from the mean discharge rate during the trial period, the period during which neural activity was significantly elevated with a predetermined confidence level was identified in each spike train. In certain neurons, bursts of action potentials were identified by determining the period in each spike train in which the activation deviated most from the expected Poisson distribution. Using this method, we related these defined periods of modulation to saccade initiation in specific cell types recorded in FEF and SEF. Cells were recorded in SEF while monkeys made saccades to targets presented alone. Cells were recorded in FEF while monkeys made saccades to targets presented alone or with surrounding distractors. There were no significant differences in the time-course of activity of the population of FEF presaccadic movement cells prior to saccades generated to singly presented or distractor-embedded targets. The discharge of presaccadic movement cells in FEF and SEF could be subdivided quantitatively into an early prelude followed by a high-rate burst of activity that occurred at a consistent interval before saccade initiation. The time of burst onset relative to saccade onset in SEF presaccadic movement cells was earlier and more variable than in FEF presaccadic movement cells. The termination of activity of another population of SEF neurons, known as preparatory set cells, was time-locked to saccade initiation. In addition, the cessation of SEF preparatory set cell activity coincided precisely with the beginning of the burst of SEF presaccadic movement cells. This finding raises the possibility that SEF preparatory set cells may be involved in saccade initiation by regulating the activation of SEF presaccadic movement cells. These results demonstrate the utility of the Poisson spike train analysis to relate periods of neuronal modulation to behavior.

Search Efficiency but Not Response Interference Affects Visual Selection in Frontal Eye Field

Two manipulations of a visual search task were used to test the hypothesis that the discrimination of a target from distractors by visually responsive neurons in the frontal eye field (FEF) marks the outcome and conclusion of visual processing instead of saccade preparation. First, search efficiency was reduced by increasing the similarity of the distractors to the target. Second, response interference was introduced by infrequently changing the location of the target in the array. Both manipulations increased reaction time, but only the change in search efficiency affected the time needed to select the target by visually responsive neurons. This result indicates that visually responsive neurons in FEF form an explicit representation of the location of the target in the image.

The detection of visual signals by macaque frontal eye field during masking

The neural link between a sensory signal and its behavioral report was investigated in macaques trained to locate an intermittently detectable visual target. Neurons in the frontal eye field, an area involved in converting the outcome of visual processing into motor commands, responded at short latencies to the target stimulus whether or not the monkey reported its presence. Neural activity immediately preceding the visual response to the mask was significantly greater on hits than on misses, and was significantly greater on false alarms than on correct rejections. The results show that visual signals masked by light are not filtered out at early stages of visual processing; furthermore, the magnitude of early visual responses in prefrontal cortex predicts the behavioral report.

Dynamics of saccade target selection: Race model analysis of double step and search step saccade production in human and macaque

We investigated how saccade target selection by humans and macaque monkeys reacts to unexpected changes of the image. This was explored using double step and search step tasks in which a target, presented alone or as a singleton in a visual search array, steps to a different location on infrequent, random trials. We report that human and macaque monkey performance are qualitatively indistinguishable. Performance is stochastic with the probability of producing a compensated saccade to the final target location decreasing with the delay of the step. Compensated saccades to the final target location are produced with latencies relative to the step that are comparable to or less than the average latency of saccades on trials with no target step. Noncompensated errors to the initial target location are produced with latencies less than the average latency of saccades on trials with no target step. Noncompensated saccades to the initial target location are followed by corrective saccades to the final target location following an intersaccade interval that decreases with the interval between the target step and the initiation of the noncompensated saccade. We show that this pattern of results cannot be accounted for by a race between two stochastically independent processes producing the saccade to the initial target location and another process producing the saccade to the final target location. However, performance can be accounted for by a race between three stochastically independent processes--a GO process producing the saccade to the initial target location, a STOP process interrupting that GO process, and another GO process producing the saccade to the final target location. Furthermore, if the STOP process and second GO process start at the same time, then the model can account for the incidence and latency of mid-flight corrections and rapid corrective saccades. This model provides a computational account of saccade production when the image changes unexpectedly.

Measurements of Simultaneously Recorded Spiking Activity and Local Field Potentials Suggest that Spatial Selection Emerges in the Frontal Eye Field

The frontal eye field (FEF) participates in selecting the location of behaviorally relevant stimuli for guiding attention and eye movements. We simultaneously recorded local field potentials (LFPs) and spiking activity in the FEF of monkeys performing memory-guided saccade and covert visual search tasks. We compared visual latencies and the time course of spatially selective responses in LFPs and spiking activity. Consistent with the view that LFPs represent synaptic input, visual responses appeared first in the LFPs followed by visual responses in the spiking activity. However, spatially selective activity identifying the location of the target in the visual search array appeared in the spikes about 30 ms before it appeared in the LFPs. Because LFPs reflect dendritic input and spikes measure neuronal output in a local brain region, this temporal relationship suggests that spatial selection necessary for attention and eye movements is computed locally in FEF from spatially nonselective inputs.

Antecedents and correlates of visual detection and awareness in macaque prefrontal cortex

We have investigated the neural basis of visual detection in monkeys trained to report the presence or absence of a visual stimulus that was rendered intermittently detectable by backward masking. Neurons were recorded in the frontal eye field (FEF), an area located in prefrontal cortex that is involved in converting the outcome of visual processing into a command to shift gaze. The behavioral and neuronal data were analyzed in terms of signal detection theory. We found that the initial visual responses in FEF provided signals that could form the basis for correct or erroneous detection of the target. A later phase of prolonged elevated activity occurred in many visual neurons and all movement neurons that was highly correlated with the monkeys report of target presence. When observed in movement cells that project to oculomotor structures, this period of activation is interpreted as a motor command leading to the behavioral response. When observed in visual cells that do not project to oculomotor structures, the later period of activation does not admit to the motor command interpretation. Because the visual neurons likely contribute to the feedback pathway to visual cortical areas, we hypothesize that the later selective activation in the prefrontal visual neurons interacts with ongoing activity in visual cortical areas contributing to the process by which a particular sensory representation receives enhanced activation and thereby engages attention and awareness.

The Effect of Visual Search Efficiency on Response Preparation Neurophysiological Evidence for Discrete Flow

Most models assume that response time (RT) comprises the time required for successive processing stages, but they disagree about whether information is transmitted continuously or discretely between stages. We tested these alternative hypotheses by measuring when movement-related activity began in the frontal eye field (FEF) of macaque monkeys performing visual search. Previous work showed that RT was longer when visual neurons in FEF took longer to select the target, a finding consistent with prolonged perceptual processing during less efficient search. We now report that the buildup of saccadic movement-related activity in FEF is delayed in inefficient visual search. Variability in the delay of movement-related activity accounted for the difference in RT between search conditions and for the variability of RT within conditions. These findings provide neurophysiological support for the hypothesis that information is transmitted discretely between perceptual and response stages of processing during visual search.

Effect of target-distractor similarity on FEF visual selection in the absence of the target

We tested the hypothesis that frontal eye field (FEF) visual activity integrates visual information with a template of a target by examining whether a target that is not present in a search display influences the target selection in FEF. Neural activity was recorded in FEF of macaque monkeys performing visual search for a singleton target defined by color or direction of motion. The target remained constant throughout, but not across experimental sessions. Trials with distractors dissimilar to the target were interleaved with trials with distractors similar to the target. The hypothesis was tested by measuring the magnitude of activity in randomly interleaved trials with the target absent and only distractors in the display. We found that the response to the distractors was significantly greater when presented with displays consisting of distractors that resembled the absent target than when presented with displays consisting of distractors most different from the absent target. The influence of target-distractor similarity on FEF activity was also observed when the target was present, as reported previously. These data suggest that a template of the absent target can influence the selection process in FEF. This provides more direct evidence that FEF integrates visual information and knowledge of the target to determine the goal of a saccade.