Biology subjects

Schall, J. D.

Publications and source records attributed to Schall, J. D..

26 records · Page 2Linked to original sources

bioRxiv2019

Neural correlates of goal-directed and non-goal-directed movements

What are the neural correlates that distinguish goal-directed (G) from non-goal-directed movements (nG)? We investigated this question in the monkey frontal eye field, which is implicated in voluntary control of saccades. We found that only for G-saccades, the variability in spike rate across trials decreased, the regularity of spike timings within trials increased, the neural activity increased earlier from baseline and had a concurrent reduction of LFP beta band power.

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bioRxiv2019

Neural Mechanisms for Executive Control of Speed-Accuracy Tradeoff

The balance of speed with accuracy requires error detection and performance adaptation. To date, neural concomitants of these processes have been investigated only with noninvasive measures. To provide the first neurophysiological description, macaque monkeys performed visual search under cued speed accuracy tradeoff (SAT). Monkeys changed SAT emphasis immediately after a cued switch while neuron discharges were sampled in medial frontal cortex area supplementary eye field (SEF). A multiplicity of SEF neurons signaled production of choice errors and timing errors. Modulation of SEF activity after choice errors predicted production of un-rewarded corrective saccades. Modulation of activity after timing errors signaled reward prediction error. Adaptation of performance during SAT of visual search was accomplished through pronounced changes in neural state from before search array presentation until after reward delivery. These results contextualize previous findings using noninvasive measures, complement neurophysiological findings in visuomotor structures, endorse the role of medial frontal cortex as a critic relative to the actor instantiated in visuomotor structures, and extend our understanding of the distributed neural mechanisms of SAT.\n\nHIGHLIGHTSO_LIMedial frontal cortex enables post-error adjustment during SAT\nC_LIO_LIChoice and timing errors were signaled by partially overlapping neural pools\nC_LIO_LIMedial frontal cortex can proactively modulate visuomotor processes\nC_LIO_LIMedial frontal cortex is to visuomotor circuits as critic to actor\nC_LI

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bioRxiv2019

Sequential Operations Revealed by Serendipitous Feature Selectivity in Frontal Eye Field

Neurons in macaque frontal eye field contribute to spatial but typically not feature selection during visual search. Using an innovative visual search task, we report a serendipitous discovery that some frontal eye field neurons can develop rapid selectivity for stimulus orientation that is used to guide gaze during a visual search task with pro-saccade and anti-saccade responses. This feature selectivity occurs simultaneously at multiple locations for all objects sharing that feature and coincides with when neurons select the singleton of a search array. This feature selectivity also reveals the distinct, subsequent operation of selecting the endpoint of the saccade in pro-saccade as well as anti-saccade trials. These results demonstrate that target selection preceding saccade preparation is composed of multiple operations. We conjecture that singleton selection indexes the allocation of attention, which can be divided, to conspicuous items. Consequently, endpoint selection indexes the focused allocation of attention to the endpoint of the saccade. These results demonstrate that saccade target selection is not a unitary process.\n\nSIGNIFICANCE STATEMENTFrontal eye field is well known to contribute to spatial selection for attention and eye movements. We discovered that some frontal eye field neurons can acquire selectivity for stimulus orientation when it guides visual search. The chronometry of neurons with and without feature selectivity reveal distinct operations accomplishing visual search.

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bioRxiv2017

Functional categories in macaque frontal eye field

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 cluster outcomes vary with analysis assumptions, consensus clustering aggregates over multiple cluster 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 ten functional categories, expanding on the traditional three. Categories were distinguished by latency, magnitude, and sign of visual response, presence of sustained activity, and 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 provides better information guiding microcircuit models of cortical function.\n\nSIGNIFICANCE STATEMENTThe contribution of a brain region cannot be understood without knowing the diversity, arrangement, and circuitry of constituent neurons. Traditional descriptions of frontal eye field include visual, visuo-saccadic, and saccadic categories. Here, we employ a novel consensus clustering method to identify more reliably functional categories in neural data. While confirming the traditional categories, consensus clustering distinguishes additional, previously unappreciated diversity in neural activity patterns. Such information is necessary to formulate correct microcircuit models of cortical function.

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bioRxiv2017

Neural mechanisms of speed-accuracy tradeoff of visual search: Saccade vigor, targeting errors, 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, and 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. Visually-responsive neurons modulated baseline firing rate and the time course of salience evidence. Unlike FEF, the magnitude of visual responses in SC did not vary across SAT conditions, but the time to locate the target was longer in Accurate as compared to Fast trials. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Search errors occurred when visual salience neurons in FEF and SC treated distractors as targets, even in the Accurate condition. Saccade-related neural activity in SC but less FEF varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT.\n\nSignificance statementNeurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This paper 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.

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bioRxiv2017

Prefrontal control of visual distraction

Avoiding distraction by salient irrelevant stimuli is critical to accomplishing daily tasks. Regions of prefrontal cortex control attention by enhancing the representation of task-relevant information in sensory cortex, which can be measured directly in modulation of both single neurons and averaging of the scalp-recorded electroencephalogram [1,2]. However, when irrelevant information is particularly conspicuous, it may distract attention and interfere with the selection of behaviorally relevant information. Many studies have shown that that distraction can be minimized via top-down control [3-5], but the cognitive and neural mechanisms giving rise to this control over distraction remain uncertain and vigorously debated [6-8]. Bridging neurophysiology to electrophysiology, we simultaneously recorded neurons in prefrontal cortex and event-related potentials (ERPs) over extrastriate visual cortex to track the processing of salient distractors during a visual search task. Critically, we observed robust suppression of salient distractor representations in both cortical areas, with suppression arising in prefrontal cortex before being manifest in the ERP signal over extrastriate cortex. Furthermore, only prefrontal neurons that participated in selecting the task-relevant target also showed suppression of the task-irrelevant distractor. This suggests a common prefrontal mechanism for target selection and distractor suppression, with input from prefrontal cortex being responsible for both selecting task-relevant and suppressing task-irrelevant information in sensory cortex. Taken together, our results resolve a long-standing debate over the mechanisms that prevent distraction, and provide the first evidence directly linking suppressed neural firing in prefrontal cortex with surface ERP measures of distractor suppression.

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bioRxiv2017

Microcircuitry of Performance Monitoring

AcknowledgmentsThis work was supported by R01-MH55806, P30-EY08126, and by Robin and Richard Patton through the E. Bronson Ingram Chair in Neuroscience. We thank J. Easley M. Feurtado, M. Maddox, P. Middlebrooks, S. Motorny, J. Parker, M. Schall, C.R. Subraveti, A. Tomarken, and L. Toy for animal care and other technical assistance. We thank J. Brown, M. Cox, K. Dougherty, S. Errington, A. Maier, V. Stuphorn, A. Tomarken, and J. Westerberg for helpful discussions and comments on the manuscript.\n\nConflicts of interestNone\n\nCortical circuit mechanisms in medial frontal cortex enabling executive control are unknown. Hence, in monkeys performing a saccade countermanding task to earn larger or smaller fluid rewards, we sampled spiking and synaptic activity simultaneously across all layers of the supplementary eye field (SEF), an agranular cortical area contributing to performance monitoring in nonhuman primate and human studies. Laminar-specific synaptic currents with associated spike rate facilitation and suppression represented error production, reward gain or loss feedback, and reward delivery. The latency, polarity and magnitude of current and spike rate modulation were not predicted by the canonical cortical microcircuit. Pronounced synaptic currents in layer 2/3, which are modulated by loss magnitude, will contribute to the error-related negativity (ERN) and feedback-related negativity (FRN). These unprecedented findings reveal critical features of the cortical microcircuitry supporting performance monitoring and demonstrate that SEF can contribute to the error- and feedback-related negativity.\n\nSubject termscountermanding, stop signal task, goal selection, response inhibition, executive control, canonical cortical microcircuit, error-related negativity, reinforcement learning, reward prediction error

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bioRxiv2017

Unification of Countermanding and Perceptual Decision-making

Perceptual decision-making, studied using two-alternative forced-choice tasks, is explained by sequential sampling models of evidence accumulation, which correspond to the dynamics of neurons in sensorimotor structures of the brain12. Response inhibition, studied using stop-signal (countermanding) tasks, is explained by a race model of the initiation or canceling of a response, which correspond to the dynamics of neurons in sensorimotor structures34. Neither standard model accounts for performance of the other task. Sequential sampling models incorporate response initiation as an uninterrupted non-decision time parameter independent of task-related variables. The countermanding race model does not account for the choice process. Here we show with new behavioral, neural and computational results that perceptual decision making of varying difficulty can be countermanded with invariant efficiency, that single prefrontal neurons instantiate both evidence accumulation and response inhibition, and that an interactive race between two GO and one STOP stochastic accumulator fits countermanding choice behavior. Thus, perceptual decision-making and response control, previously regarded as distinct mechanisms, are actually aspects of more flexible behavior supported by a common neural and computational mechanism. The identification of this aspect of decision-making with response production clarifies the component processes of decision-making.

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