Difficulty of visual search modulates neuronal interactions and response variability in the frontal eye field (original) (raw)
Related papers
2010
Numerous studies have described different functional cell types in the frontal eye field (FEF), but the reliability of the distinction between these types has been uncertain. Studies in other brain areas have described specific differences in the width of action potentials recorded from different cell types. To substantiate the functionally defined cell types encountered in FEF, we measured the width of spikes of visual, movement, and visuomovement types of FEF neurons in macaque monkeys. We show that visuomovement neurons had the thinnest spikes, consistent with a role in local processing. Movement neurons had the widest spikes, consistent with their role in sending eye movement commands to subcortical structures such as the superior colliculus. Visual neurons had wider spikes than visuomovement neurons, consistent with their role in receiving projections from occipital and parietal cortex. These results show how structure and function of FEF can be linked to guide inferences about neuronal architecture. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341: 95-116, 1994. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99 -104, 1990. Constantinidis C, Goldman-Rakic PS. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J Neurophysiol 88: 3487-3497, 2002. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19: 274 -287, 1999. DiCarlo JJ, Maunsell JH. Using neuronal latency to determine sensory-motor processing pathways in reaction time tasks. J Neurophysiol 93: 2974 -2986, 2005. Dow BM. Functional classes of cells and their laminar distribution in monkey visual cortex. J Neurophysiol 37: 927-946, 1974. Fries W. Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230: 55-76, 1984. Goldberg ME, Bushnell MC. Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. J Neurophysiol 46: 773-787, 1981. González-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA. Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953, 2005. Gur M, Beylin A, Snodderly DM. Physiological properties of macaque V1
Nelson MJ, Murthy A, Schall JD. Neural control of visual search by frontal eye field: chronometry of neural events and race model processes..—We investigated the chronometry of neural processes in frontal eye fields of macaques performing double-step saccade visual search in which a conspicuous target changes location in the array on a random fraction of trials. Durations of computational processes producing a saccade to original and final target locations (GO1 and GO2, respectively) are derived from response times (RT) on different types of trials. In these data, GO2 tended to be faster than GO1, demonstrating that inhibition of the initial saccade did not delay production of the compensated saccade. Here, we measured the dynamics of visual, visuomovement, and movement neuron activity in relation to these processes by examining trials when neurons instantiated either process. First, we verified that saccades were initiated when the discharge rate of movement neurons reached a threshold that was invariant across RT and trial type. Second, the time when visual and visuomovement neurons selected the target and when movement neuron activity began to accumulate were not significantly different across trial type. Third, the interval from the beginning of accumulation to threshold of movement-related activity was significantly shorter when instantiating the GO2 relative to the GO1 process. Differences observed between monkeys are discussed. Fourth, random variation of RT was accounted for to some extent by random variation in both the onset and duration of selective activity of each neuron type but mostly by variation of movement neuron accumulation duration. These findings offer new insights into the sources of control of target selection and saccade production in dynamic environments. diffusion model; linking hypothesis; linking proposition; perceptual decision; decision making WHEN WE ARE PRESENTED WITH a typical cluttered visual scene, the production of a gaze shift to the location of a target item entails neural and supervenient psychological processes. According to one theoretical framework, these processes are comprised of distinct computational stages accomplishing the dissociable subtasks needed to select the target and
Reliability of Macaque Frontal Eye Field Neurons Signaling Saccade Targets during Visual Search
2001
Although many studies have explored the neural correlates of visual attention and selection, few have examined the reliability with which neurons represent relevant information. We monitored activity in the frontal eye field (FEF) of monkeys trained to make a saccade to a target defined by the conjunction of color and shape or to a target defined by color differences. The difficulty of conjunction search was manipulated by varying the number of distractors, and the difficulty of feature search was manipulated by varying the similarity in color between target and distractors. The reliability of individual neurons in signaling the target location in correct trials was determined using a neuron-anti-neuron approach within a winner-take-all architecture. On average, approximately seven trials of the activity of single neurons were sufficient to match near-perfect behavioral performance in the easiest search, and ϳ14 trials were sufficient in the most difficult search. We also determined how many neurons recorded separately need to be evaluated within a trial to match behavioral performance. Results were quantitatively similar to those of the single neuron analysis. We also found that signal reliability in the FEF did not change with task demands, and overall, behavioral accuracy across the search tasks was approximated when only six trials or neurons were combined. Furthermore, whether combining trials or neurons, the increase in time of target discrimination corresponded to the increase in mean saccade latency across visual search difficulty levels. Finally, the variance of spike counts in the FEF increased as a function of the mean spike count, and the parameters of this relationship did not change with attentional selection.
Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets
eLife, 2018
In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while i...
Predictive Activity in Macaque Frontal Eye Field Neurons During Natural Scene Searching
Journal of Neurophysiology, 2010
Generating sequences of multiple saccadic eye movements allows us to search our environment quickly and efficiently. Although the frontal eye field cortex (FEF) has been linked to target selection and making saccades, little is known about its role in the control and performance of the sequences of saccades made during self-guided visual search. We recorded from FEF cells while monkeys searched for a target embedded in natural scenes and examined the degree to which cells with visual and visuo-movement activity showed evidence of target selection for future saccades. We found that for about half of these cells, activity during the fixation period between saccades predicted the next saccade in a sequence at an early time that precluded selection based on current visual input to a cell's response field. In addition to predicting the next saccade, activity during the fixation prior to two successive saccades also predicted the direction and goal of the second saccade in the sequenc...
Timing of Target Discrimination in Human Frontal Eye Fields
Journal of Cognitive Neuroscience, 2004
& Frontal eye field (FEF) neurons discharge in response to behaviorally relevant stimuli that are potential targets for saccades. Distinct visual and motor processes have been dissociated in the FEF of macaque monkeys, but little is known about the visual processing capacity of FEF in humans. We used double-pulse transcranial magnetic stimulation [(d)TMS] to investigate the timing of target discrimination during visual conjunction search. We applied dual TMS pulses separated by 40 msec over the right FEF and vertex. These were applied in five timing conditions to sample separate time windows within the first 200 msec of visual processing. (d)TMS impaired search performance, reflected in reduced d 0 scores. This effect was limited to a time window between 40 and 80 msec after search array onset. These parameters correspond with single-cell activity in FEF that predicts monkeys' behavioral reports on hit, miss, false alarm, and correct rejection trials. Our findings demonstrate a crucial early role for human FEF in visual target discrimination that is independent of saccade programming. & D
Neural Basis of the Set-Size Effect in Frontal Eye Field: Timing of Attention During Visual Search
Journal of Neurophysiology, 2009
Visual search for a target object among distractors often takes longer when more distractors are present. To understand the neural basis of this capacity limitation, we recorded activity from visually-responsive neurons in the frontal eye field of macaque monkeys searching for a target among distractors defined by form (randomly oriented T or L). To test the hypothesis that the delay of response time with increasing number of distractors originates in the delay of attention allocation by frontal eye field neurons, we manipulated the number of distractors presented with the search target. When monkeys were presented with more distractors, visual target selection was delayed and neuronal activity was reduced in proportion to longer response time. These findings indicate that the time taken by frontal eye field eurons to select the target contributes to the variation in visual search efficiency. Balan PF, Oristaglio J, Schneider DM, Gottlieb J. Neuronal correlates of the set-size effect in monkey lateral intraparietal area. PLoS Biol 6: e158, 2008. Basso MA, Wurtz RH. Modulation of neuronal activity in superior colliculus by changes in target probability. J Neurosci 18: 7519-7534, 1998. Bergen JR, Julesz B. Parallel versus serial processing in rapid pattern discrimination. Nature 303: 696-698, 1983. Bichot NP, Schall JD. Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci 2: 549-554, 1999. Bichot NP, Thompson KG, Rao SC, Schall JD. Reliability of frontal eye field neurons signaling saccade targets during visual search. J Neurosci 21: 713-725, 2001. Bisley JW, Goldberg ME. Neuronal activity in the lateral intraparietal area and spatial attention. Science 299: 81-86, 2003. Bruce CJ, Goldberg ME. Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603-635, 1985. Bundesen C. A theory of visual attention. Psychol Rev 97: 523-547, 1990. Bundesen C, Habekost T, Kyllingsbaek S. A neural theory of visual attention: bridging cognition and neurophysiology. Psychol Rev 112: 291-328, 2005. Carrasco M, Yeshurun Y. The contribution of covert attention to the set-size and eccentricity effects in visual search. J Exp Psychol Hum Percept Perform 24: 673-692, 1998. Constantinidis C, Steinmetz MA. Neuronal responses in area 7a to multiple-stimulus displays: I. Neurons encode the location of the salient stimulus. Cereb Cortex 11: 581-591, 2001. Desimone R, Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci 18: 193-222, 1995. Duncan J, Humphreys GW. Visual search and stimulus similarity. Psychol Rev 96: 433-458, 1989. Funahashi S, Bruce CJ, Goldman-Rakic PS. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61: 331-349, 1989.
Effects of Stimulus-Response Compatibility on Neural Selection in Frontal Eye Field
Neuron, 2003
when FEF neurons select the target from distractors Department of Psychology marks the outcome and conclusion of stimulus encoding Vanderbilt University and selection (Thompson et al., 1996). 111 21st Avenue South Supporting this hypothesis, we have shown that al-301 Wilson Hall though search efficiency and response interference both Nashville, Tennessee 37240 affect RT, only search efficiency affects the time when neurons select the target (Sato et al., 2001). While persuasive, these findings do not completely exclude the Summary possibility that the target selection by FEF neurons corresponds to saccade preparation. More conclusive evi-We investigated the neural basis of visual and saccade dence requires manipulation of stimulus-response mapselection in the frontal eye field of macaque monkeys ping to explicitly decouple stimulus encoding and using a singleton search task with prosaccade or antiresponse preparation (Kornblum et al., 1990). saccade responses. Two types of neurons were distin-For this study, monkeys were trained to produce a guished. The first initially selected the singleton even prosaccade or an antisaccade in response to an elonin antisaccade trials, although most subsequently segated color singleton in a visual search array (Figure lected the endpoint of the saccade. The time the single-1A). If the selection of the target in a search array by ton was located was not affected by stimulus-response FEF neurons corresponds to the selection of the location compatibility and did not vary with reaction time of the singleton, then the singleton should be selected across trials. The second type of neuron selected only regardless of the direction of the gaze shift at a time the endpoint of the saccade. The time of endpoint that should not be influenced by stimulus-response selection by these neurons accounted for most of the compatibility (Figure 1B, left). On the other hand, if target effect of stimulus-response compatibility on reaction selection by FEF neurons corresponds to preparation time. These results indicate that visual selection and of the saccade, then only the endpoint of the saccade saccade selection are different processes. should be selected regardless of the position of the singleton at a time that should vary with RT according Introduction to stimulus-response compatibility (Figure 1B, right). We found both types of neurons in FEF. This suggests that Measures of reaction time (RT) provide insights into the visual selection and saccade selection are distinguishdynamics and architecture of human cognition. Many able processes. models assume that tasks are performed by a sequence A preliminary report of some of these data has apof more or less distinct processes such as stimulus peared (T. Sato et al., 2002, Soc. Neurosci., abstract). encoding, memory retrieval, and response preparation (reviewed in Meyer et al., 1988). Several studies devel-Results oped means to manipulate and identify these processes (reviewed in Sternberg, 2001), but ultimately the struc-Behavioral Data ture of covert processes cannot be deduced solely from Table 1 presents the mean RT for three monkeys in the timing of overt responses. Event-related potentials prosaccade and antisaccade trials. RT was significantly have provided additional insights about the covert prolonger in antisaccade trials than in prosaccade trials. cesses (e.g., McCarthy and Donchin, 1981; Coles et al.,
The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process—target-step reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys' response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation.