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

Philos Trans R Soc Lond B Biol Sci. 2013 Sep 9;368(1628):20130071. doi: 10.1098/rstb.2013.0071. Print 2013 Oct 19.

Abstract

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.

Keywords: computational models; frontal eye field; perceptual decision-making; speed–accuracy trade-off; visual attention; visual search.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Chronobiology Phenomena / physiology*
  • Decision Making / physiology*
  • Eye Movements / physiology*
  • Macaca
  • Models, Neurological*
  • Pattern Recognition, Visual / physiology*
  • Species Specificity
  • Stochastic Processes
  • Visual Fields / physiology*