Neural mechanisms for executive control of speed-accuracy trade-off.

The medial frontal cortex (MFC) plays an important but disputed role in speed-accuracy trade-off (SAT). In samples of neural spiking in the supplementary eye field (SEF) in the MFC simultaneous with the visuomotor frontal eye field and superior colliculus in macaques performing a visual search with instructed SAT, during accuracy emphasis, most SEF neurons discharge less from before stimulus presentation until response generation. Discharge rates adjust immediately and simultaneously across structures upon SAT cue changes. SEF neurons signal choice errors with stronger and earlier activity during accuracy emphasis. Other neurons signal timing errors, covarying with adjusting response time. Spike correlations between neurons in the SEF and visuomotor areas did not appear, disappear, or change sign across SAT conditions or trial outcomes. These results clarify findings with noninvasive measures, complement previous neurophysiological findings, and endorse the role of the MFC as a critic for the actor instantiated in visuomotor structures.

Neural mechanisms of speed-accuracy tradeoff of visual search: saccade vigor, the origin of targeting errors, and comparison of the superior colliculus and frontal eye field.

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 speed-accuracy tradeoff: history, physiology, methodology, and behavior.

There are few behavioral effects as ubiquitous as the speed-accuracy tradeoff (SAT). From insects to rodents to primates, the tendency for decision speed to covary with decision accuracy seems an inescapable property of choice behavior. Recently, the SAT has received renewed interest, as neuroscience approaches begin to uncover its neural underpinnings and computational models are compelled to incorporate it as a necessary benchmark. The present work provides a comprehensive overview of SAT. First, I trace its history as a tractable behavioral phenomenon and the role it has played in shaping mathematical descriptions of the decision process. Second, I present a "users guide" of SAT methodology, including a critical review of common experimental manipulations and analysis techniques and a treatment of the typical behavioral patterns that emerge when SAT is manipulated directly. Finally, I review applications of this methodology in several domains.

Neural chronometry and coherency across speed-accuracy demands reveal lack of homomorphism between computational and neural mechanisms of evidence accumulation.

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.

Neural mechanisms of speed-accuracy tradeoff.

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.

Response variability of frontal eye field neurons modulates with sensory input and saccade preparation but not visual search salience.

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.

Homologous mechanisms of visuospatial working memory maintenance in macaque and human: properties and sources.

Although areas of frontal cortex are thought to be critical for maintaining information in visuospatial working memory, the event-related potential (ERP) index of maintenance is found over posterior cortex in humans. In the present study, we reconcile these seemingly contradictory findings. Here, we show that macaque monkeys and humans exhibit the same posterior ERP signature of working memory maintenance that predicts the precision of the memory-based behavioral responses. In addition, we show that the specific pattern of rhythmic oscillations in the alpha band, recently demonstrated to underlie the human visual working memory ERP component, is also present in monkeys. Next, we concurrently recorded intracranial local field potentials from two prefrontal and another frontal cortical area to determine their contribution to the surface potential indexing maintenance. The local fields in the two prefrontal areas, but not the cortex immediately posterior, exhibited amplitude modulations, timing, and relationships to behavior indicating that they contribute to the generation of the surface ERP component measured from the distal posterior electrodes. Rhythmic neural activity in the theta and gamma bands during maintenance provided converging support for the engagement of the same brain regions. These findings demonstrate that nonhuman primates have homologous electrophysiological signatures of visuospatial working memory to those of humans and that a distributed neural network, including frontal areas, underlies the posterior ERP index of visuospatial working memory maintenance.

Neural mechanisms of saccade target selection: gated accumulator model of the visual-motor cascade.

We review a new computational model developed to understand how evidence about stimulus salience in visual search is translated into a saccade command. The model uses the activity of visually responsive neurons in the frontal eye field as evidence for stimulus salience that is accumulated in a network of stochastic accumulators to produce accurate and timely saccades. We discovered that only when the input to the accumulation process was gated could the model account for the variability in search performance and predict the dynamics of movement neuron discharge rates. This union of cognitive modeling and neurophysiology indicates how the visual-motor transformation can occur, and provides a concrete mapping between neuron function and specific cognitive processes.

Neurally constrained modeling of perceptual decision making.

Stochastic accumulator models account for response time in perceptual decision-making tasks by assuming that perceptual evidence accumulates to a threshold. The present investigation mapped the firing rate of frontal eye field (FEF) visual neurons onto perceptual evidence and the firing rate of FEF movement neurons onto evidence accumulation to test alternative models of how evidence is combined in the accumulation process. The models were evaluated on their ability to predict both response time distributions and movement neuron activity observed in monkeys performing a visual search task. Models that assume gating of perceptual evidence to the accumulating units provide the best account of both behavioral and neural data. These results identify discrete stages of processing with anatomically distinct neural populations and rule out several alternative architectures. The results also illustrate the use of neurophysiological data as a model selection tool and establish a novel framework to bridge computational and neural levels of explanation.

Neural correlates of correct and errant attentional selection revealed through N2pc and frontal eye field activity.

The goal of this study was to obtain a better understanding of the physiological basis of errors of visual search. Previous research has shown that search errors occur when visual neurons in the frontal eye field (FEF) treat distractors as if they were targets. We replicated this finding during an inefficient form search and extended it by measuring simultaneously a macaque homologue of an event-related potential indexing the allocation of covert attention known as the m-N2pc. Based on recent work, we expected errors of selection in FEF to propagate to areas of extrastriate cortex responsible for allocating attention and implicated in the generation of the m-N2pc. Consistent with this prediction, we discovered that when FEF neurons selected a distractor instead of the search target, the m-N2pc shifted in the same, incorrect direction prior to the erroneous saccade. This suggests that such errors are due to a systematic misorienting of attention from the initial stages of visual processing. Our analyses also revealed distinct neural correlates of false alarms and guesses. These results demonstrate that errant gaze shifts during visual search arise from errant attentional processing.

Cooperation and competition among frontal eye field neurons during visual target selection.

The role of spike rate versus timing codes in visual target selection is unclear. We simultaneously recorded activity from multiple frontal eye field neurons and asked whether they interacted to select targets from distractors during visual search. When both neurons in a pair selected the target and had overlapping receptive fields (RFs), they cooperated more than when one or neither neuron in the pair selected the target, measured by positive spike timing correlations using joint peristimulus time histogram analysis. The amount of cooperation depended on the location of the search target: it was higher when the target was inside both neurons' RFs than when it was inside one RF but not the other, or outside both RFs. Elevated spike timing coincidences occurred at the time of attentional selection of the target as measured by average modulation of discharge rates. We observed competition among neurons with spatially non-overlapping RFs, measured by negative spike timing correlations. Thus, we provide evidence for dynamic and task-dependent cooperation and competition among frontal eye field neurons during visual target selection.

Working memory capacity is decreased in sleep-deprived internal medicine residents.

BACKGROUND: Concerns about medical errors due to sleep deprivation during residency training led the Accreditation Council for Graduate Medical Education to mandate reductions in work schedules. Although call rotations with extended shifts continue, effects on resident sleep-wake times and working memory capacity (WMC) have not been investigated. OBJECTIVES: The objective of this study was to measure effects of call rotations on sleep-wake times and WMC in internal medicine residents. METHODS: During 2 months of an internal medicine training program adhering to ACGME work-hour restrictions (between April 2006 and June 2007), residents completed daily WMC tests, wore actigraphy watches, and logged their sleep hours. This observational study was conducted during a call month requiring 30-hour call rotations every fourth night, whereas the noncall month, which allowed sleep/wake cycle freedom, was used as the control. MAIN OUTCOME MEASURES: Sleep hours per night and WMC testing. RESULTS: Thirty-nine residents completing the study had less sleep per night during their call month (6.4 vs 7.3 h per night noncall, p < 0.001) and sleep per night varied from 3.7 to 10.1 hours. Call rotation caused greater self-assessed sleepiness and reduced WMC recall scores (-2.6/test, p < 0.05), and more math errors occurred when on call (+1.07/test, p < 0.04). Full recovery of WMC did not occur until the fourth day after call. On-call rotation on the first month had a confounding detrimental effect on WMC. CONCLUSION: A month of call rotations reduced overall sleep per night; sleep hours per night were variable, and WMC was adversely affected. Decreased WMC could explain impaired judgment during sleep deprivation, although clinical error rates were not evaluated.

On the origin of event-related potentials indexing covert attentional selection during visual search.

Despite nearly a century of electrophysiological studies recording extracranially from humans and intracranially from monkeys, the neural generators of nearly all human event-related potentials (ERPs) have not been definitively localized. We recorded an attention-related ERP component, known as the N2pc, simultaneously with intracranial spikes and local field potentials (LFPs) in macaques to test the hypothesis that an attentional-control structure, the frontal eye field (FEF), contributed to the generation of the macaque homologue of the N2pc (m-N2pc). While macaques performed a difficult visual search task, the search target was selected earliest by spikes from single FEF neurons, later by FEF LFPs, and latest by the m-N2pc. This neurochronometric comparison provides an empirical bridge connecting macaque and human experiments and a step toward localizing the neural generator of this important attention-related ERP component.

Complex working memory span tasks and higher-order cognition: a latent-variable analysis of the relationship between processing and storage.

Complex span tasks, assumed by many to measure an individual's working memory capacity, are predictive of several aspects of higher-order cognition. However, the underlying cause of the relationships between "processing-and-storage" tasks and cognitive abilities is still hotly debated nearly 30 years after the tasks were first introduced. The current study utilised latent constructs across verbal, numerical, and spatial content domains to examine a number of questions regarding the predictive power of complex span tasks. In particular, the relations among processing time, processing accuracy, and storage accuracy from the complex span tasks were examined, in combination with their respective relationships with fluid intelligence. The results point to a complicated pattern of unique and shared variance among the constructs. Implications for various theories of working memory are discussed.

Neural basis of the set-size effect in frontal eye field: timing of attention during visual search.

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 (FEF) 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 FEF 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 FEF neurons to select the target contributes to the variation in visual search efficiency.

A touch screen based Stop Signal Response Task in rhesus monkeys for studying impulsivity associated with chronic cocaine self-administration.

Among a range of cognitive deficits, human cocaine addicts display increased impulsivity and decreased performance monitoring. In order to establish an animal model that can be used to study the underlying neurobiology of these deficits associated with addiction, we have developed a touch screen based Stop Signal Response Task for rhesus monkeys. This task is essentially identical to the clinically used Stop Signal Task employed for diagnostic and research purposes. In this task, impulsivity is reflected in the amount of time needed to inhibit a response after it has been initiated, the Stop Signal Response Time (SSRT). Performance monitoring is reflected by the slowing of response times following Stop trials (Post-Stop Slowing, PSS). Herein we report on the task structure, the staged methods for training animals to perform the task, and a comparison of performance values for control and cocaine experienced animals. Relative to controls, monkeys that had self-administered cocaine, followed by 18 months abstinence, displayed increased impulsivity (increased SSRT values), and decreased performance monitoring (decreased PSS values). Our results are consistent with human data, and thereby establish an ideal animal model for studying the etiology and underlying neurobiology of cocaine-induced impulse control and performance monitoring deficits.

Biophysical support for functionally distinct cell types in the frontal eye field.

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.

The importance of temporal distinctiveness for forgetting over the short term.

Rapidly forgetting information once attention is diverted seems to be a ubiquitous phenomenon. The cause of this rapid decline has been debated for decades; some researchers claim that memory traces decay as a function of time out of the focus of attention, whereas others claim that prior memory traces cause confusability by interfering with the current trace. Here we demonstrate that performance after a long delay can be better than performance after a short delay if the temporal confusability between the current item and previous items is reduced. These results provide strong evidence for the importance of temporal confusability, rather than decay, as the cause of forgetting over the short term.

Effects of incentive on working memory capacity: behavioral and pupillometric data.

We evaluated the hypothesis that individual differences in working memory capacity are explained by variation in mental effort, persons with low capacity exerting less effort than persons with high capacity. Groups previously rated high and low in working memory capacity performed the reading span task under three levels of incentive. The effort hypothesis holds that low span subjects exert less effort during task performance than do high spans. Subjects' pupil sizes were recorded online during task performance as a measure of mental effort. Both recall performance and pupil diameter were found to be increased under incentives, but were additive with span (incentives increased performance and pupil diameter equivalently for both span groups). Contrary to the effort hypothesis, task-evoked pupillary responses indicated that if anything, low span subjects exert more effort than do high spans.