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Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

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Abstract

Saccades require a spatiotemporal transformation of activity between the intermediate layers of the superior colliculus (iSC) and downstream brainstem burst generator. The dynamic linear ensemble-coding model (Goossens and Van Opstal 2006) proposes that each iSC spike contributes a fixed mini-vector to saccade displacement. Although biologically-plausible, this model assumes cortical areas like the frontal eye fields (FEF) simply provide the saccadic goal to be executed by the iSC and brainstem burst generator. However, the FEF and iSC operate in unison during saccades, and a pathway from the FEF to the brainstem burst generator that bypasses the iSC exists. Here, we investigate the impact of large yet reversible inactivation of the FEF on iSC activity in the context of the model across four saccade tasks. We exploit the overlap of saccade vectors generated when the FEF is inactivated or not, comparing the number of iSC spikes for metrically-matched saccades. We found that the iSC emits fewer spikes for metrically-matched saccades during FEF inactivation. The decrease in spike count is task-dependent, with a greater decrease accompanying more cognitively-demanding saccades. Our results show that FEF integrity influences the readout of iSC activity in a task-dependent manner. We propose that the dynamic linear ensemble-coding model be modified so that FEF inactivation increases the gain of a readout parameter, effectively increasing the influence of a single iSC spike. We speculate that this modification could be instantiated by FEF and iSC pathways to the cerebellum that could modulate the excitability of the brainstem burst generator.

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Acknowledgements

This work was supported by operating grants from the Canadian Institutes of Health Research to BDC (MOPs: 93796, 123247 and 142317) and the Natural Sciences and Engineering Research Council (NSERC; RGPIN-311680). TRP was supported by an Ontario Graduate Scholarship and TRP and SD were supported by funding from an NSERC CREATE grant.

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Authors and Affiliations

  1. Département de neurosciences, Université de Montréal, Montréal, QC, Canada

    Tyler R. Peel

  2. The Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada

    Suryadeep Dash & Brian D. Corneil

  3. Department of Physiology & Pharmacology, University of Western Ontario, London, ON, Canada

    Suryadeep Dash & Brian D. Corneil

  4. Department of Psychology, McGill University, Montréal, QC, Canada

    Stephen G. Lomber

  5. Department of Psychology, University of Western Ontario, London, ON, Canada

    Brian D. Corneil

  6. Robarts Research Institute, 1151 Richmond St N, London, ON, N6A 5B7, Canada

    Brian D. Corneil

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  1. Tyler R. Peel
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Correspondence to Brian D. Corneil.

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Significance statement

One of the enduring puzzles in the oculomotor system is how it achieves the spatiotemporal transformation, converting spatial activity within the intermediate layers of the superior colliculus (iSC) into a rate code within the brainstem burst generator. The spatiotemporal transformation has traditionally been viewed as the purview of the oculomotor brainstem. Here, within the context of testing a biologically-plausible model of the spatiotemporal transformation, we show that reversible inactivation of the frontal eye fields (FEF) decreases the number of spikes issued by the iSC for metrically-matched saccades, with greater decreases accompanying more cognitively-demanding tasks. These results show that signals from the FEF influence the spatiotemporal transformation.

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Peel, T.R., Dash, S., Lomber, S.G. et al. Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner. J Comput Neurosci 49, 229–249 (2021). https://doi.org/10.1007/s10827-020-00760-7

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