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Stochastic accumulator models account for response times and errors in perceptual decision making by assuming a noisy accumulation of perceptual evidence to a threshold. Previously, we explained saccade visual search decision making by macaque monkeys with a stochastic multiaccumulator model in which accumulation was driven by a gated feed-forward integration to threshold of spike trains from visually responsive neurons in frontal eye field that signal stimulus salience. This neurally constrained model quantitatively accounted for response times and errors in visual search for a target among varying numbers of distractors and replicated the dynamics of presaccadic movement neurons hypothesized to instantiate evidence accumulation. This modeling framework suggested strategic control over gate or over threshold as two potential mechanisms to accomplish speed-accuracy tradeoff (SAT). Here, we show that our gated accumulator model framework can account for visual search performance under SAT instructions observed in a milestone neurophysiological study of frontal eye field. This framework captured key elements of saccade search performance, through observed modulations of neural input, as well as flexible combinations of gate and threshold parameters necessary to explain differences in SAT strategy across monkeys. However, the trajectories of the model accumulators deviated from the dynamics of most presaccadic movement neurons. These findings demonstrate that traditional theoretical accounts of SAT are incomplete descriptions of the underlying neural adjustments that accomplish SAT, offer a novel mechanistic account of decision-making mechanisms during speed-accuracy tradeoff, and highlight questions regarding the identity of model and neural accumulators. NEW & NOTEWORTHY A gated accumulator model is used to elucidate neurocomputational mechanisms of speed-accuracy tradeoff. Whereas canonical stochastic accumulators adjust strategy only through variation of an accumulation threshold, we demonstrate that strategic adjustments are accomplished by flexible combinations of both modulation of the evidence representation and adaptation of accumulator gate and threshold. The results indicate how model-based cognitive neuroscience can translate between abstract cognitive models of performance and neural mechanisms of speed-accuracy tradeoff.
PURPOSE - The purpose of this study was to report a case of optic disc cupping reversal in an adult without significant intraocular pressure-lowering treatment.
PATIENT - A 20-year-old female with a history of mild juvenile open-angle glaucoma who developed subjective blurred vision and a decrease in cupping of her optic discs.
RESULTS - Dilated examination demonstrated decreased cup-to-disc ratios in both eyes with a slight blurring of the disc margin in the right eye. The appearance of both optic discs returned to baseline after weight loss therapy.
CONCLUSIONS - An unexplained reduction of optic nerve cup-to-disc ratio should prompt a workup for other etiologies, such as increased intracranial pressure. Baseline photographs not subjected to computerized scan obsolescence are extremely useful in monitoring the long-term appearance of asymmetric optic discs as an adjunct to the clinical examination.
Frontal eye field (FEF) in macaque monkeys contributes to visual attention, visual-motor transformations and production of eye movements. Traditionally, neurons in FEF have been classified by the magnitude of increased discharge rates following visual stimulus presentation, during a waiting period, and associated with eye movement production. However, considerable heterogeneity remains within the traditional visual, visuomovement, and movement categories. Cluster analysis is a data-driven method of identifying self-segregating groups within a dataset. Because many cluster analysis techniques exist and outcomes vary with analysis assumptions, consensus clustering aggregates over multiple analyses, identifying robust groups. To describe more comprehensively the neuronal composition of FEF, we applied a consensus clustering technique for unsupervised categorization of patterns of spike rate modulation measured during a memory-guided saccade task. We report 10 functional categories, expanding on the traditional 3 categories. Categories were distinguished by latency, magnitude, and sign of visual response; the presence of sustained activity; and the dynamics, magnitude and sign of saccade-related modulation. Consensus clustering can include other metrics and can be applied to datasets from other brain regions to provide better information guiding microcircuit models of cortical function.
Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In "Accurate" relative to "Fast" trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. NEW & NOTEWORTHY Neurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This article reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision making.
The dorsal lateral geniculate nucleus of the thalamus (LGN) receives the main outputs of both eyes and relays those signals to the visual cortex. Each retina projects to separate layers of the LGN so that each LGN neuron is innervated by a single eye. In line with this anatomical separation, visual responses of almost all of LGN neurons are driven by one eye only. Nonetheless, many LGN neurons are sensitive to what is shown to the other eye as their visual responses differ when both eyes are stimulated compared to when the driving eye is stimulated in isolation. This, predominantly suppressive, binocular modulation of LGN responses might suggest that the LGN is the first location in the primary visual pathway where the outputs from the two eyes interact. Indeed, the LGN features several anatomical structures that would allow for LGN neurons responding to one eye to modulate neurons that respond to the other eye. However, it is also possible that binocular response modulation in the LGN arises indirectly as the LGN also receives input from binocular visual structures. Here we review the extant literature on the effects of binocular stimulation on LGN spiking responses, highlighting findings from cats and primates, and evaluate the neural circuits that might mediate binocular response modulation in the LGN.
© 2018 Wiley Periodicals, Inc.
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.
Copyright © 2016 the American Physiological Society.
The stochastic accumulation framework provides a mechanistic, quantitative account of perceptual decision-making and how task performance changes with experimental manipulations. Importantly, it provides an elegant account of the speed-accuracy trade-off (SAT), which has long been the litmus test for decision models, and also mimics the activity of single neurons in several key respects. Recently, we developed a paradigm whereby macaque monkeys trade speed for accuracy on cue during visual search task. Single-unit activity in frontal eye field (FEF) was not homomorphic with the architecture of models, demonstrating that stochastic accumulators are an incomplete description of neural activity under SAT. This paper summarizes and extends this work, further demonstrating that the SAT leads to extensive, widespread changes in brain activity never before predicted. We will begin by reviewing our recently published work that establishes how spiking activity in FEF accomplishes SAT. Next, we provide two important extensions of this work. First, we report a new chronometric analysis suggesting that increases in perceptual gain with speed stress are evident in FEF synaptic input, implicating afferent sensory-processing sources. Second, we report a new analysis demonstrating selective influence of SAT on frequency coupling between FEF neurons and local field potentials. None of these observations correspond to the mechanics of current accumulator models.
Intelligent agents balance speed of responding with accuracy of deciding. Stochastic accumulator models commonly explain this speed-accuracy tradeoff by strategic adjustment of response threshold. Several laboratories identify specific neurons in prefrontal and parietal cortex with this accumulation process, yet no neurophysiological correlates of speed-accuracy tradeoff have been described. We trained macaque monkeys to trade speed for accuracy on cue during visual search and recorded the activity of neurons in the frontal eye field. Unpredicted by any model, we discovered that speed-accuracy tradeoff is accomplished through several distinct adjustments. Visually responsive neurons modulated baseline firing rate, sensory gain, and the duration of perceptual processing. Movement neurons triggered responses with activity modulated in a direction opposite of model predictions. Thus, current stochastic accumulator models provide an incomplete description of the neural processes accomplishing speed-accuracy tradeoffs. The diversity of neural mechanisms was reconciled with the accumulator framework through an integrated accumulator model constrained by requirements of the motor system.
Copyright © 2012 Elsevier Inc. All rights reserved.
Event-related potentials (ERPs) have provided crucial data concerning the time course of psychological processes, but the neural mechanisms producing ERP components remain poorly understood. This study continues a program of research in which we investigated the neural basis of attention-related ERP components by simultaneously recording intracranially and extracranially from macaque monkeys. Here, we compare the timing of attentional selection by the macaque homologue of the human N2pc component (m-N2pc) with the timing of selection in the frontal eye field (FEF), an attentional-control structure believed to influence posterior visual areas thought to generate the N2pc. We recorded FEF single-unit spiking and local field potentials (LFPs) simultaneously with the m-N2pc in monkeys performing an efficient pop-out search task. We assessed how the timing of attentional selection depends on task demands by direct comparison with a previous study of inefficient search in the same monkeys (e.g., finding a T among Ls). Target selection by FEF spikes, LFPs, and the m-N2pc was earlier during efficient pop-out search rather than during inefficient search. The timing and magnitude of selection in all three signals varied with set size during inefficient but not efficient search. During pop-out search, attentional selection was evident in FEF spiking and LFP before the m-N2pc, following the same sequence observed during inefficient search. These observations are consistent with the hypothesis that feedback from FEF modulates neural activity in posterior regions that appear to generate the m-N2pc even when competition for attention among items in a visual scene is minimal.
Discharge rate modulation of frontal eye field (FEF) neurons has been identified with a representation of visual search salience (physical conspicuity and behavioral relevance) and saccade preparation. We tested whether salience or saccade preparation are evident in the trial-to-trial variability of discharge rate. We quantified response variability via the Fano factor in FEF neurons recorded in monkeys performing efficient and inefficient visual search tasks. Response variability declined following stimulus presentation in most neurons, but despite clear discharge rate modulation, variability did not change with target salience. Instead, we found that response variability was modulated by stimulus luminance and the number of items in the visual field independently of attentional demands. Response variability declined to a minimum before saccade initiation, and presaccadic response variability was directionally tuned. In addition, response variability was correlated with the response time of memory-guided saccades. These results indicate that the trial-by-trial response variability of FEF neurons reflects saccade preparation and the strength of sensory input, but not visual search salience or attentional allocation.