scholarly journals Neural chronometry and coherency across speed–accuracy demands reveal lack of homomorphism between computational and neural mechanisms of evidence accumulation

2013 ◽  
Vol 368 (1628) ◽  
pp. 20130071 ◽  
Author(s):  
Richard P. Heitz ◽  
Jeffrey D. Schall

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.

2017 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall

AbstractBalancing 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.Significance 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.


2019 ◽  
Vol 121 (4) ◽  
pp. 1300-1314 ◽  
Author(s):  
Mathieu Servant ◽  
Gabriel Tillman ◽  
Jeffrey D. Schall ◽  
Gordon D. Logan ◽  
Thomas J. Palmeri

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.


Author(s):  
Thomas J. Palmeri ◽  
Jeffrey D. Schall ◽  
Gordon D. Logan

Mathematical psychology and systems neuroscience have converged on stochastic accumulator models to explain decision making. We examined saccade decisions in monkeys while neurophysiological recordings were made within their frontal eye field. Accumulator models were tested on how well they fit response probabilities and distributions of response times to make saccades. We connected these models with neurophysiology. To test the hypothesis that visually responsive neurons represented perceptual evidence driving accumulation, we replaced perceptual processing time and drift rate parameters with recorded neurophysiology from those neurons. To test the hypothesis that movement related neurons instantiated the accumulator, we compared measures of neural dynamics with predicted measures of accumulator dynamics. Thus, neurophysiology both provides a constraint on model assumptions and data for model selection. We highlight a gated accumulator model that accounts for saccade behavior during visual search, predicts neurophysiology during search, and provides insights into the locus of cognitive control over decisions.


2005 ◽  
Vol 94 (1) ◽  
pp. 605-611 ◽  
Author(s):  
Jason D. Connolly ◽  
Melvyn A. Goodale ◽  
Herbert C. Goltz ◽  
Douglas P. Munoz

Variation in response latency to identical sensory stimuli has been attributed to variation in neural activity mediating preparatory set. Here we report evidence for a relationship between saccadic reaction time (SRT) and set-related brain activity measured with event-related functional magnetic resonance imaging. We measured hemodynamic activation time-courses during a preparatory “gap” period, during which no visual stimulus was present and no saccades were made. The subjects merely anticipated appearance of the target. Saccade direction and latency were recorded during scanning, and trials were sorted according to SRT. Both the frontal (FEF) and supplementary eye fields showed pretarget preparatory activity, but only in the FEF was this activity correlated with SRT. Activation in the intraparietal sulcus did not show any preparatory activity. These data provide evidence that the human FEF plays a central role in saccade initiation; pretarget activity in this region predicts both the type of eye movement (whether the subject will look toward or away from the target) and when a future saccade will occur.


2018 ◽  
Vol 120 (1) ◽  
pp. 372-384 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall

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.


2018 ◽  
Author(s):  
Markus Ostarek ◽  
Jeroen van Paridon ◽  
Falk Huettig

AbstractProcessing words with referents that are typically observed up or down in space (up/down words) influences the subsequent identification of visual targets in congruent locations. Eye-tracking studies have shown that up/down word comprehension shortens launch times of subsequent saccades to congruent locations and modulates concurrent saccade trajectories. This can be explained by a task-dependent interaction of semantic processing and oculomotor programs or by a direct recruitment of direction-specific processes in oculomotor and spatial systems as part of semantic processing. To test the latter possibility, we conducted a functional magnetic resonance imaging experiment and used multi-voxel pattern analysis to assess 1) whether the typical location of word referents can be decoded from the fronto-parietal spatial network and 2) whether activity patterns are shared between up/down words and up/down saccadic eye movements. In line with these hypotheses, significant decoding of up vs. down words and cross-decoding between up/down saccades and up/down words were observed in the frontal eye field region in the superior frontal sulcus and the inferior parietal lobule. Beyond these spatial attention areas, typical location of word referents could be decoded from a set of occipital, temporal, and frontal areas, indicating that interactions between high-level regions typically implicated with lexical-semantic processing and spatial/oculomotor regions constitute the neural basis for access to spatial aspects of word meanings.


Author(s):  
Kaleb A. Lowe ◽  
Wolf Zinke ◽  
M. Anthony Phipps ◽  
Josh Cosman ◽  
Micala Maddox ◽  
...  

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