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Relation of frontal eye field activity to saccade initiation during a countermanding task

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Abstract

The countermanding (or stop signal) task probes the control of the initiation of a movement by measuring subjects’ ability to withhold a movement in various degrees of preparation in response to an infrequent stop signal. Previous research found that saccades are initiated when the activity of movement-related neurons reaches a threshold, and saccades are withheld if the growth of activity is interrupted. To extend and evaluate this relationship of frontal eye field (FEF) activity to saccade initiation, two new analyses were performed. First, we fit a neurometric function that describes the proportion of trials with a stop signal in which neural activity exceeded a criterion discharge rate as a function of stop signal delay, to the inhibition function that describes the probability of producing a saccade as a function of stop signal delay. The activity of movement-related but not visual neurons provided the best correspondence between neurometric and inhibition functions. Second, we determined the criterion discharge rate that optimally discriminated between the distributions of discharge rates measured on trials when saccades were produced or withheld. Differential activity of movement-related but not visual neurons could distinguish whether a saccade occurred. The threshold discharge rates determined for individual neurons through these two methods agreed. To investigate how reliably movement-related activity predicted movement initiation; the analyses were carried out with samples of activity from increasing numbers of trials from the same or from different neurons. The reliability of both measures of initiation threshold improved with number of trials and neurons to an asymptote of between 10 and 20 movement-related neurons. Combining the activity of visual neurons did not improve the reliability of predicting saccade initiation. These results demonstrate how the activity of a population of movement-related but not visual neurons in the FEF contributes to the control of saccade initiation. The results also validate these analytical procedures for identifying signals that control saccade initiation in other brain structures.

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Notes

  1. In asking how many neurons prepare a saccade one discovers a specific lack of information about density and number of neurons in various structures. However, a back-of-the-envelope calculation is possible. We start with an estimate of 73,000 neurons/mm2 based on the count of 146,000 cells per mm2 of cerebral cortex with other estimates from as low as 20,000 neurons/mm2 to as high as 92,000 neurons/mm2 (Rockel et al. 1980; Braitenberg and Schüz 1991). Lacking information to the contrary, we will assume equivalent density for all relevant structures. The structures we considered in which presaccadic activity related to the timing of the initiation of the movement has been reported are the frontal eye field, superior colliculus, thalamus, basal ganglia and brainstem. We take the cortical area of FEF to be 50 mm2, so assuming a uniform 2 mm cortical depth, the total cell number in FEF is 7,300,000 (low 2,000,000; high 9,200,000). However, if only the pyramidal cells in layer 5 are responsible for saccade generation, then this count must be reduced proportionally by estimating the depth of layer 5 at 0.05 mm—182,500 (low 50,000; high 230,000). Estimates for the superior colliculus derived from direct counts using new methods (Herculano-Houzel et al. 2007). are that there are ~7,000,000 total cells in the SC with about 25% of those being neurons. Assuming the intermediate layers constitute 40% of the depth of the SC and that 50% of the neurons in the intermediate layers contribute to saccade generation, the number of neurons is 350,000. Restricting the thalamus contribution to the lateral sector of the medial dorsal nucleus and assuming again that 50% of these neurons contribute to saccade generation, the number is 100,000. Assuming that the number of neurons in the caudate nucleus and the substantia nigra pars reticulata that contribute to saccade generation are equivalent to that in the superior colliculus, then the basal ganglia number is 700,000. Finally, we assume that there are 10,000 long-lead burst neurons in the brainstem. Based on all these assumptions and estimates, the total number of presaccadic movement-related neurons amounts to 9.9 × 105. Now, not all of these neurons will be active before a given saccade. If we assume that one third of the neurons are active before any saccade, then the total is 3.3 × 105, and if the fraction is as low as one tenth, then the total is 9.9 × 104. This is the basis for our claim that 105–106 neurons are necessary for initiation of a saccade.

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Acknowledgments

We are grateful to A. Evans, J. Jewett, K. Reis and C. Wiley for assistance preparing the manuscript. This work was supported by Robin and Richard Patton through the E. Bronson Ingram Chair of Neuroscience and grants RO1-MH55806, P30-EY08126, P30-HD015052.

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Authors and Affiliations

  1. Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Department of Psychology, Vanderbilt University, Nashville, TN, 37203, USA

    Joshua W. Brown, Doug P. Hanes, Jeffrey D. Schall & Veit Stuphorn

  2. Department of Psychological and Brain Sciences, Indiana University, 1101 E Tenth St., Bloomington, IN, 47405, USA

    Joshua W. Brown

  3. The Zanvyl Krieger Mind/Brain Institute and The Department of Psychological and Brain Sciences, Johns Hopkins University, 362 Krieger Hall, 3400 N. Charles Street, Baltimore, MD, 21218, USA

    Veit Stuphorn

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  1. Joshua W. Brown
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Correspondence to Joshua W. Brown.

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Brown, J.W., Hanes, D.P., Schall, J.D. et al. Relation of frontal eye field activity to saccade initiation during a countermanding task. Exp Brain Res 190, 135–151 (2008). https://doi.org/10.1007/s00221-008-1455-0

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