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The unknown but knowable relationship between Presaccadic Accumulation of activity and Saccade initiation

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Abstract

The goal of this short review is to call attention to a yawning gap of knowledge that separates two processes essential for saccade production. On the one hand, knowledge about the saccade generation circuitry within the brainstem is detailed and precise – push-pull interactions between gaze-shifting and gaze-holding processes control the time of saccade initiation, which begins when omnipause neurons are inhibited and brainstem burst neurons are excited. On the other hand, knowledge about the cortical and subcortical premotor circuitry accomplishing saccade initiation has crystalized around the concept of stochastic accumulation – the accumulating activity of saccade neurons reaching a fixed value triggers a saccade. Here is the gap: we do not know how the reaching of a threshold by premotor neurons causes the critical pause and burst of brainstem neurons that initiates saccades. Why this problem matters and how it can be addressed will be discussed. Closing the gap would unify two rich but curiously disconnected empirical and theoretical domains.

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References

  • Antoniades, C. A., & Kennard, C. (2015). Ocular motor abnormalities in neurodegenerative disorders. Eye (Lond)., 29, 200–207.

    Article  CAS  PubMed  Google Scholar 

  • Barbe, M. T., Monyer, H., & Bruzzone, R. (2006). Cell-cell communication beyond connexins: The pannexin channels. Physiology, 21, 103–114.

    Article  CAS  PubMed  Google Scholar 

  • Bergeron, A., & Guitton, D. (2002). In multiple-step gaze shifts: Omnipause (OPNs) and collicular fixation neurons encode gaze position error; OPNs gate saccades. Jornal of Neurophysiology, 88, 1726–1742.

    Article  Google Scholar 

  • Bogacz, R., Wagenmakers, E. J., Forstmann, B. U., & Nieuwenhuis, S. (2010). The neural basis of the speed-accuracy tradeoff. Trends in Neurosciences, 33, 10–16.

    Article  CAS  PubMed  Google Scholar 

  • Bompas, A., Campbell, A. E., & Sumner, P. (2020). Cognitive control and automatic interference in mind and brain: A unified model of saccadic inhibition and countermanding. Psychological Review, 127, 524–561.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boucher, L., Palmeri, T. J., Logan, G. D., & Schall, J. D. (2007). Inhibitory control in mind and brain: An interactive race model of countermanding saccades. Psychological Review, 114, 376–397.

    Article  PubMed  Google Scholar 

  • Bozis, A., & Moschovakis, A. K. (1998). Neural network simulations of the primate oculomotor system. III. An one-dimensional, one-directional model of the superior colliculus. Biological cybernetics, 79, 215–230.

    Article  CAS  PubMed  Google Scholar 

  • Büttner-Ennever, J. A., Cohen, B., Pause, M., & Fries, W. (1988). Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man. The Journal of Comparative Neurology, 267, 307–321.

    Article  PubMed  Google Scholar 

  • Buttner-Ennever, J. A., Horn, A. K., Henn, V., & Cohen, B. (1999). Projections from the superior colliculus motor map to omnipause neurons in monkey. The Journal of Comparative Neurology, 413, 55–67.

    Article  CAS  PubMed  Google Scholar 

  • Camalier, C. R., Gotler, A., Murthy, A., Thompson, K. G., Logan, G. D., Palmeri, T. J., & Schall, J. D. (2007). Dynamics of saccade target selection: Race model analysis of double step and search step saccade production in human and macaque. Vision Research, 47, 2187–2211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen, B., & Henn, V. (1972). Unit activity in the pontine reticular formation associated with eye movements. Brain Research, 46, 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Condorelli, D. F., Belluardo, N., Trovato-Salinaro, A., & Mudò, G. (2000). Expression of Cx36 in mammalian neurons. Brain Research Brain Research Reviews, 32, 72–85.

    Article  CAS  Google Scholar 

  • Costello, M. G., Zhu, D., Salinas, E., & Stanford, T. R. (2013). Perceptual modulation of motor–but not visual–responses in the frontal eye field during an urgent-decision task. Journal of Neuroscience, 33, 16394–16408.

    Article  CAS  PubMed  Google Scholar 

  • Crapse, T. B., Lau, H., & Basso, M. A. (2018). A role for the superior colliculus in decision criteria. Neuron., 97, 181–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cromer, J.A., & Waitzman, D.M. (2006) Neurones associated with saccade metrics in the monkey central mesencephalic reticular formation. The Journal of Physiology 570, 507-523

  • Daye, P. M., Optican, L. M., Roze, E., et al. (2013). Neuromimetic model of saccades for localizing deficits in an atypical eye-movement pathology. Journal of Translational Medicine, 11, 125.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daye, P. M., Optican, L. M., Blohm, G., & Lefèvre, P. (2014). Hierarchical control of two-dimensional gaze saccades. Journal of Computational Neuroscience, 36, 355–382.

    Article  PubMed  Google Scholar 

  • Ding, L., & Gold, J. I. (2010). Caudate encodes multiple computations for perceptual decisions. Journal of Neuroscience, 30, 15747–15759.

    Article  CAS  Google Scholar 

  • Drugowitsch, J., Moreno-Bote, R., Churchland, A. K., Shadlen, M. N., & Pouget, A. (2012). The cost of accumulating evidence in perceptual decision making. Journal of Neuroscience, 32, 3612–3628.

    Article  CAS  PubMed  Google Scholar 

  • Evans, N. J., Hawkins, G. E., Boehm, U., Wagenmakers, E. J., & Brown, S. D. (2017). The computations that support simple decision-making: a comparison between the diffusion and urgency-gating models. Scientific Reports, 7, 1-13.

  • Everling, S., & Munoz, D. P. (2000). Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. Journal of Neuroscience, 20, 387–400.

    Article  CAS  PubMed  Google Scholar 

  • Everling, S., Dorris, M. C., Klein, R. M., & Munoz, D. P. (1999). Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. Journal of Neuroscience, 19, 2740–2754.

    Article  CAS  PubMed  Google Scholar 

  • Everling, S., Paré, M., Dorris, M. C., & Munoz, D. P. (1998). Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: implications for control of fixation and saccade behavior. Journal of Neurophysiology, 79, 511–528.

    Article  CAS  PubMed  Google Scholar 

  • Evinger, C., Kaneko, C. R., & Fuchs, A. F. (1982). Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. Journal of Neurophysiology, 47, 827–844.

    Article  CAS  PubMed  Google Scholar 

  • Fecteau, J. H., & Munoz, D. P. (2007). Warning signals influence motor processing. Journal of Neurophysiology, 97, 1600–1609.

    Article  PubMed  Google Scholar 

  • Forstmann, B. U., Ratcliff, R., & Wagenmakers, E.-J. (2016). Sequential sampling models in cognitive neuroscience: advantages, applications, and extensions. Annual Review of Psychology, 67, 641–666.

    Article  CAS  PubMed  Google Scholar 

  • Gandhi, N. J., & Keller, E. L. (1997). Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. Journal of Neurophysiology, 78, 2221–2225.

    Article  CAS  PubMed  Google Scholar 

  • Godlove, D. C., & Schall, J. D. (2016). Microsaccade production during saccade cancelation in a stop-signal task. Vision Research, 118, 5–16.

    Article  PubMed  Google Scholar 

  • Godlove, D. C., Garr, A. K., Woodman, G. F., & Schall, J. D. (2011). Measurement of the extraocular spike potential during saccade countermanding. Journal of Neurophysiology, 106, 104–114.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goffart, L., Hafed, Z. M., & Krauzlis, R. J.  (2012) Visual fixation as equilibrium: Evidence from superior colliculus inactivation. Journal of Neuroscience 32, 10627-10636

  • Hafed Z. M., Goffart L., & Krauzlis R. J. (2008). Superior colliculus inactivation causes stable offsets in eye position during tracking. Journal of Neuroscience, 28, 8124-8137.

  • Hafed, Z.M., Krauzlis, R.J., (2012) Similarity of superior colliculus involvement in microsaccade and saccade generation. Journal of Neurophysiology 107, 1904-1916

  • Handel, A., & Glimcher, P. W. (1997). Response properties of saccade-related burst neurons in the central mesencephalic reticular formation. Journal of Neurophysiology, 78, 2164–2175.

    Article  CAS  PubMed  Google Scholar 

  • Hanes, D.P., Patterson, W.F. 2nd, & Schall, J.D. (1998). Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. Journal of Neurophysiology 79, 817-834.

  • Hanes, D.P., & Schall, J.D. (1996). Neural control of voluntary movement initiation. Science, 274, 427-430.

  • Hanks, T., et al. (2014). A neural mechanism of speed-accuracy tradeoff in macaque area LIP. eLife, 3, e02260.

  • Hauser, C. K., Zhu, D., Stanford, T. R., & Salinas, E. (2018). Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets. Elife, 7, e33456.

    Article  PubMed  PubMed Central  Google Scholar 

  • Heitz, R. P., & Schall, J. D. (2012). Neural mechanisms of speed-accuracy tradeoff. Neuron, 76, 616–628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hikosaka, O., & Wurtz, R. H. (1985). Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. Journal of Neurophysiology, 53, 266–291.

    Article  CAS  PubMed  Google Scholar 

  • Hikosaka, O., & Wurtz, R. H. (1985). Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. Journal of Neurophysiology, 53, 292–308.

    Article  CAS  PubMed  Google Scholar 

  • Horn, A. K., Büttner-Ennever, J. A., Wahle, P., & Reichenberger, I. (1994). Neurotransmitter profile of saccadic omnipause neurons in nucleus raphe interpositus. Journal of Neuroscience, 14, 2032–2046.

    Article  CAS  PubMed  Google Scholar 

  • Huerta, M. F., & Kaas, J. H. (1990). Supplementary eye field as defined by intracortical microstimulation: connections in macaques. Journal of Comparative Neurology, 293, 299–330.

    Article  CAS  PubMed  Google Scholar 

  • Huerta, M. F., Krubitzer, L. A., & Kaas, J. H. (1986). Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys: I. Subcortical connections. Journal of Comparative Neurology, 253, 415–439.

    Article  CAS  PubMed  Google Scholar 

  • Izawa, Y., Suzuki, H., & Shinoda, Y. (2009). Response properties of fixation neurons and their location in the frontal eye field in the monkey. Journal of Neurophysiology, 102, 2410–2422.

    Article  PubMed  Google Scholar 

  • Izawa, Y., Suzuki, H., & Shinoda, Y. (2005). Initiation and suppression of saccades by the frontal eye field in the monkey. Annals of the New York Academy of Sciences, 1039, 220–231.

    Article  PubMed  Google Scholar 

  • Jantz, J. J., Watanabe, M., Everling, S., & Munoz, D. P. (2013). Threshold mechanism for saccade initiation in frontal eye field and superior colliculus. Journal of Neurophysiology, 109, 2767–2780.

    Article  PubMed  Google Scholar 

  • Kanda, T., Iwamoto, Y., Yoshida, K., & Shimazu, H. (2007). Glycinergic inputs cause the pause of pontine omnipause neurons during saccades. Neuroscience Letters, 413, 16–20.

    Article  CAS  PubMed  Google Scholar 

  • Kaneko, C. R. (2006). Saccade-related, long-lead burst neurons in the monkey rostral pons. Journal of Neurophysiology, 95(2), 979–994.

    Article  PubMed  Google Scholar 

  • Kaneko, C. R. (1996). Effects of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. Journal of Neurophysiology, 75, 2229–2242.

    Article  CAS  PubMed  Google Scholar 

  • Keller, E. L. (1974). Participation of medial pontine reticular formation in eye movement generation in monkey. Journal of Neurophysiology, 37, 316–332.

    Article  CAS  PubMed  Google Scholar 

  • Keller, E. L., & Edelman, J. A. (1994). Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. Journal of Neurophysiology, 72, 2754–2770.

    Article  CAS  PubMed  Google Scholar 

  • Keller, E.L., Lee, B.T., Lee, K.M. (2008). Frontal eye field signals that may trigger the brainstem saccade generator. Progress in Brain Research, 171, 107-114.

  • Kobayashi, Y., Saito, Y., & Isa, T. (2001). Facilitation of saccade initiation by brainstem cholinergic system. Brain Development, 23(Suppl 1), S24–S27.

    Article  PubMed  Google Scholar 

  • Krahe, R., & Gabbiani, F. (2004). Burst firing in sensory systems. Nature Reviews Neuroscience, 5, 13–23.

    Article  CAS  PubMed  Google Scholar 

  • Krauzlis, R.J., Basso, M.A., Wurtz, R.H. (1997). Shared motor error for multiple eye movements. Science. 276, 1693-1695.

  • Krauzlis, R. J., Goffart, L., & Hafed, Z. M. (2017). Neuronal control of fixation and fixational eye movements. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160205.

    Article  Google Scholar 

  • Lefevre, P., Quaia, C., & Optican, L. M. (1998). Distributed model of control of saccades by superior colliculus and cerebellum. Neural Networks, 11, 1175–1190.

    Article  PubMed  Google Scholar 

  • Lisman, J. E. (1997). Bursts as a unit of neural information: making unreliable synapses reliable. Trends in Neurosciences, 20, 38–43.

    Article  CAS  PubMed  Google Scholar 

  • Lo, C. C., & Wang, X. J. (2006). Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nature Neuroscience, 9, 956–963.

    Article  CAS  PubMed  Google Scholar 

  • Lo, C. C., Wang, C. T., & Wang, X. J. (2015). Speed-accuracy tradeoff by a control signal with balanced excitation and inhibition. Journal of Neurophysiology, 114, 650–661.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lo, C. C., Boucher, L., Paré, M., Schall, J. D., & Wang, X. J. (2009). Proactive inhibitory control and attractor dynamics in countermanding action: a spiking neural circuit model. Journal Neuroscience, 29, 9059–9071.

    Article  CAS  PubMed  Google Scholar 

  • Logan, G. D., & Cowan, W. B. (1984). On the ability to inhibit thought and action - a theory of an act of control. Psychological Review, 91, 295–327.

    Article  Google Scholar 

  • Logan, G. D., Yamaguchi, M., Schall, J. D., & Palmeri, T. J. (2015). Inhibitory control in mind and brain 2.0: Blocked-input models of saccadic countermanding. Psychological Review, 122, 115–147.

    Article  PubMed  PubMed Central  Google Scholar 

  • Luschei, E. S., & Fuchs, A. F. (1972). Activity of brain stem neurons during eye movements of alert monkeys. Journal of Neurophysiology, 35, 445–461.

    Article  CAS  PubMed  Google Scholar 

  • Manohar, S. G., Chong, T. T., Apps, M. A., Batla, A., Stamelou, M., Jarman, P. R., et al. (2015). Reward pays the cost of noise reduction in motor and cognitive control. Current Biology, 29, 1707–1716.

    Article  CAS  Google Scholar 

  • May, P. J. (2006). The mammalian superior colliculus: Laminar structure and connections. Prog. Brain Research, 151, 321–378.

    Article  PubMed  Google Scholar 

  • Metzen, M. G., Krahe, R., & Chacron, M. J. (2016). Burst firing in the electrosensory system of gymnotiform weakly electric fish: mechanisms and functional roles. Frontiers in Computational Neuroscience, 10, 81.

    Article  PubMed  PubMed Central  Google Scholar 

  • Middlebrooks, P. G., Zandbelt, B. B., Logan, G. D., Palmeri, T. J., & Schall, J. D. (2020). Countermanding perceptual decision-making. iScience, 23(1), 100777.

    Article  PubMed  Google Scholar 

  • Miura, K., & Optican, L. M. (2006). Membrane channel properties of premotor excitatory burst neurons may underlie saccade slowing after lesions of omnipause neurons. Journal of Computational Neuroscience, 20, 25–41.

    Article  PubMed  Google Scholar 

  • Moschovakis, A. K., Karabelas, A. B., & Highstein, S. M. (1988). Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. Journal of Neurophysiology, 60, 232–262.

    Article  CAS  PubMed  Google Scholar 

  • Moschovakis, A. K., Karabelas, A. B., & Highstein, S. M. (1988). Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. Journal of Neurophysiology, 60, 263–302.

    Article  CAS  PubMed  Google Scholar 

  • Munoz, D. P., & Istvan, P. J. (1998). Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. Journal of Neurophysiology, 79, 1193–1209.

    Article  CAS  PubMed  Google Scholar 

  • Munoz, D. P., & Wurtz, R. H. (1993a). Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. Journal of Neurophysiology, 70, 559–575.

    Article  CAS  PubMed  Google Scholar 

  • Munoz, D. P., & Wurtz, R. H. (1993b). Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. Journal of Neurophysiology, 70, 576–589.

    Article  CAS  PubMed  Google Scholar 

  • Munoz, D. P., & Wurtz, R. H. (1995). Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. Journal of Neurophysiology, 73, 2313–2333.

    Article  CAS  PubMed  Google Scholar 

  • Murthy, A., Ray, S., Shorter, S. M., Schall, J. D., & Thompson, K. G. (2009). Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. Journal of Neurophysiology, 101, 2485–2506.

    Article  PubMed  PubMed Central  Google Scholar 

  • Noda, H., Sugita, S., & Ikeda, Y. (1990). Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. Journal of Comparative Neurology, 302, 330–348.

    Article  CAS  PubMed  Google Scholar 

  • O’Connell, R. G., Shadlen, M. N., Wong-Lin, K., & Kelly, S. P. (2018). Bridging neural and computational viewpoints on perceptual decision-making. Trends in Neurosciences, 41, 838–852.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ogasawara, T., Nejime, M., Takada, M., & Matsumoto, M. (2018). Primate nigrostriatal dopamine system regulates saccadic response inhibition. Neuron., 100, 1513–1526.

    Article  CAS  PubMed  Google Scholar 

  • Ohgaki, T., Curthoys, I. S., & Markham, C. H. (1987). Anatomy of physiologically identified eye-movement-related pause neurons in the cat: Pontomedullary region. Journal of Comparative Neurology, 266, 56–72.

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka, K. & Nagasaka. Y. (1999). Divergent axon collaterals from the rostral superior colliculus to the pretectal accommodation-related areas and the omnipause neuron area in the cat. The Journal of Comparative Neurology, 413, 68-76.

  • Optican, L. M. (2008). The role of omnipause neurons: Why glycine? Progress in Brain Research, 171, 115–121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Optican, L. M., & Pretegiani, E. (2017). What stops a saccade? Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160194.

    Article  Google Scholar 

  • Optican, L. M., & Pretegiani, E. (2017). A GABAergic dysfunction in the olivary-cerebellar-brainstem network may cause eye oscillations and body tremor. II. Model simulations of saccadic eye oscillations. Frontiers in Neurology, 8, 372.

    Article  PubMed  PubMed Central  Google Scholar 

  • Optican, L. M., & Quaia, C. (2002). Distributed model of collicular and cerebellar function during saccades. Annals of the New York Academy of Sciences, 956, 164–177.

    Article  PubMed  Google Scholar 

  • Optican, L. M., Rucker, J. C., Rizzo, J. R., & Hudson, T. E. (2019). Modeling gaze position-dependent opsoclonus. Progress in Brain Research, 249, 35–61.

    Article  PubMed  Google Scholar 

  • Otero-Millan, J., Macknik, S.L., Serra, A., Leigh, R.J., Martinez-Conde, S. (2011). Triggering mechanisms in microsaccade and saccade generation: a novel proposal. Annals of the New York Academy of Sciences. 1233:107-116.

  • Otero-Millan, J., Optican, L. M., Macknik, S. L., & Martinez-Conde, S. (2018). Modeling the triggering of saccades, microsaccades, and saccadic intrusions. Frontiers in Neurology, 9, 346.

  • Paré, M., & Dorris, M. C. (2011). The role of posterior parietal cortex in the regulation of saccadic eye movements. The Oxford Handbook of Eye Movements, 257-278.

  • Paré, M., & Guitton, D. (1994). The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons. Experimental Brain Research, 101, 109–122.

    PubMed  Google Scholar 

  • Paré, M., & Guitton, D. (1998). Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. Journal of Neurophysiology, 79, 3060–3076.

    Article  PubMed  Google Scholar 

  • Paré, M., Hanes, D.P. (2003). Controlled movement processing: superior colliculus activity associated with countermanded saccades. Journal of Neuroscience. 23:6480-6489.

  • Paré, M., & Munoz, D. P. (2001). Expression of a re-centering bias in saccade regulation by superior colliculus neurons. Experimental Brain Research, 137, 354–368.

    Article  PubMed  Google Scholar 

  • Paré, M., & Wurtz, R. H. (2001). Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus. Journal of Neurophysiology, 85, 2545–2562.

    Article  PubMed  Google Scholar 

  • Peltsch, A., Hemraj, A., Garcia, A., & Munoz, D. P. (2014). Saccade deficits in amnestic mild cognitive impairment resemble mild Alzheimer’s disease. European Journal of Neuroscience, 39, 2000–2013.

    Article  PubMed  Google Scholar 

  • Pretegiani, E., Rosini, F., Federico, A., Optican, L. M., & Rufa, A. (2017). Eye movements in genetic parkinsonisms affecting the α-synuclein, PARK9, and manganese network. Clinical Neurophysiology: official journal of the International Federation of Clinical Neurophysiology, 128, 2450–2453.

    Article  Google Scholar 

  • Purcell, B. A., Schall, J. D., Logan, G. D., & Palmeri, T. J. (2012). From salience to saccades: multiple-alternative gated stochastic accumulator model of visual search. Journal of Neuroscience, 32, 3433-3446.

  • Purcell, B. A., Heitz, R. P., Cohen, J. Y., Schall, J. D., Logan, G. D., & Palmeri, T. J. (2010). Neurally constrained modeling of perceptual decision making. Psychological Review, 117, 1113–1143.

    Article  PubMed  PubMed Central  Google Scholar 

  • Quaia, C., Lefevre, P., & Optican, L. M. (1999). Model of the control of saccades by superior colliculus and cerebellum. Journal of Neurophysiology, 82, 999–1018.

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishnan, A., Sureshbabu, R., & Murthy, A. (2012). Understanding how the brain changes its mind: microstimulation in the macaque frontal eye field reveals how saccade plans are changed. Journal Neuroscience, 32, 4457–4472.

    Article  CAS  PubMed  Google Scholar 

  • Ratcliff, R., Hasegawa, Y. T., Hasegawa, R. P., Smith, P. L., & Segraves, M. A. (2007). Dual diffusion model for single-cell recording data from the superior colliculus in a brightness-discrimination task. Journal of Neurophysiology, 97, 1756–1774.

    Article  PubMed  Google Scholar 

  • Raybourn, M.S., & Keller, E.L. (1977) Colliculoreticular organization in primate oculomotor system. Journal of Neurophysiology 40, 861-878

  • Reppert, T. R., Servant, M., Heitz, R. P., & Schall, J. D. (2018). Neural mechanisms of speed-accuracy tradeoff of visual search: saccade vigor, the origin of targeting errors, and comparison of the superior colliculus and frontal eye field. Journal of Neurophysiology, 120, 372-384.

  • Robinson, D. A. (1973). Models of the saccadic eye movement control system. Kybernetik, 14, 71–83.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, D. A. (1975). Oculomotor control signals. In G. Lennerstrand & P. Bach-y-Rita (Eds.), Basic Mechanisms of Ocular Motility and Their Clinical Implications (pp. 337–374). Oxford: Pergamon Press.

    Google Scholar 

  • Rodgers, C.K., Munoz, D.P., Scott, S.H., Paré, M., (2006) Discharge properties of monkey tectoreticular neurons. Journal of Neurophysiology 95, 3502-3511

  • Roitman, J. D., & Shadlen, M. N. (2002). Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. Journal Neuroscience, 22, 9475–9489.

    Article  CAS  PubMed  Google Scholar 

  • Rucci, M., & Poletti, M. (2015). Control and functions of fixational eye movements. Annual Review of Vision Science, 1, 499–518.

    Article  PubMed  PubMed Central  Google Scholar 

  • Saito, Y., & Isa, T. (2003). Local excitatory network and NMDA receptor activation generate a synchronous and bursting command from the superior colliculus. Journal Neuroscience, 23, 5854–5864.

    Article  CAS  PubMed  Google Scholar 

  • Sajad, A., Godlove, D. C., & Schall, J. D. (2019). Cortical microcircuitry of performance monitoring. Nature Neuroscience, 22, 265–274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salinas, E., & Stanford, T. R. (2018). Saccadic inhibition interrupts ongoing oculomotor activity to enable the rapid deployment of alternate movement plans. Sci Reports, 8, 14163.

    Google Scholar 

  • Schall, J. D. (2019). Accumulators, Neurons, and Response Time. Trends Neurosci, 42, 848–860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schall, J. D., Palmeri, T. J., & Logan, G. D. (2017). Models of inhibitory control. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1718), 20160193.

  • Schmidt, R., Leventhal, D. K., Mallet, N., Chen, F., & Berke, J. D. (2013). Canceling actions involves a race between basal ganglia pathways. Nature Neuroscience, 16, 1118–1124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schultz, K. P., Williams, C. R., & Busettini, C. (2010). Macaque pontine omnipause neurons play no direct role in the generation of eye blinks. Journal Neurophysiology, 103, 2255–2274.

    Article  CAS  PubMed  Google Scholar 

  • Scudder, C. A., Kaneko, C. S., & Fuchs, A. F. (2002). The brainstem burst generator for saccadic eye movements: a modern synthesis. Experimental Brain Research, 142, 439–462.

    Article  PubMed  Google Scholar 

  • Scudder, C.A., Moschovakis, A.K., Karabelas, A.B., Highstein, S.M., (1996) Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. I. Descending projections from the mesencephalon. Journal of Neurophysiology 76, 332-352

  • Segraves, M. A. (1992). Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. Journal of Neurophysiology, 68, 1967-1985.

  • Shadmehr, R., Reppert, T. R., Summerside, E. M., Yoon, T., & Ahmed, A. A. (2019). Movement vigor as a reflection of subjective economic utility. Trends in Neurosciences, 42, 323–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaikh, A. G., Ramat, S., Optican, L. M., Miura, K., Leigh, R. J., & Zee, D. S. (2008). Saccadic burst cell membrane dysfunction is responsible for saccadic oscillations. Journal of Neuro-ophthalmology: the official journal of the North American Neuro-Ophthalmology Society, 28, 329–336.

    Article  Google Scholar 

  • Shaikh, A. G., Zee, D. S., Optican, L. M., Miura, K., Ramat, S., & Leigh, R. J. (2011). The effects of ion channel blockers validate the conductance-based model of saccadic oscillations. Annals of the New York Academy of Sciences, 1233, 58–63.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherman, S. M. (2001). Tonic and burst firing: dual modes of thalamocortical relay. Trends in Neurosciences, 24, 122–126.

    Article  CAS  PubMed  Google Scholar 

  • Shinoda, Y., Sugiuchi, Y., Takahashi, M., Izawa, Y. (2011). Neural substrate for suppression of omnipause neurons at the onset of saccades. Annals of the New York Academy of Sciences. 1233:100-106.

  • Shinoda, Y., Takahashi, M., & Sugiuchi, Y. (2019). Brainstem neural circuits for fixation and generation of saccadic eye movements. Progress Brain Research, 249, 95–104.

    Article  Google Scholar 

  • Shook, B. L., Schlag‐Rey, M., & Schlag, J. (1990). Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. Journal of Comparative Neurology, 301, 618-642.

  • Sooksawate, T., Saito, Y., & Isa, T. (2005). Electrophysiological and morphological properties of identified crossed tecto-reticular neurons in the rat superior colliculus. Neuroscience Research, 52, 174–184.

    Article  PubMed  Google Scholar 

  • Sparks, D. L. (1978). Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain research, 156, 1-16.

  • Sparks, D. L. (2002). The brainstem control of saccadic eye movements. Nature Reviews Neuroscience, 3, 952–964.

    Article  CAS  PubMed  Google Scholar 

  • Spencer, R. F., Wenthold, R. J., & Baker, R. (1989). Evidence for glycine as an inhibitory neurotransmitter of vestibular, reticular, and prepositus hypoglossi neurons that project to the cat abducens nucleus. Journal of Neuroscience, 9, 2718–2736.

    Article  CAS  PubMed  Google Scholar 

  • Standage, D., Paré, M., & Blohm, G. (2018). Disinhibition as a canonical neural mechanism for flexible behavior. bioRxiv, https://doi.org/10.1101/334797

    Article  Google Scholar 

  • Standage, D., You, H., Wang, D. H., & Dorris, M. C. (2013). Trading speed and accuracy by coding time: a coupled-circuit cortical model. Plos Computational Biology 9(4), e1003021.

  • Stanton, G. B., Goldberg, M. E., & Bruce, C. J. (1988). Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology, 271, 493–506.

    Article  CAS  PubMed  Google Scholar 

  • Strassman, A., Evinger, C., McCrea, R. A., Baker, R. G., & Highstein, S. M. (1987). Anatomy and physiology of intracellularly labelled omnipause neurons in the cat and squirrel monkey. Experimental Brain Research, 67, 436–440.

    Article  CAS  PubMed  Google Scholar 

  • Stuphorn, V., & Schall, J. D. (2006). Executive control of countermanding saccades by the supplementary eye field. Nature Neuroscience, 9, 925–931.

    Article  CAS  PubMed  Google Scholar 

  • Stuphorn, V., Taylor, T.L., Schall, J.D., (2000) Performance monitoring by the supplementary eye field. Nature 408, 857-860

  • Stuphorn, V., Brown, J. W., & Schall, J. D. (2010). Role of supplementary eye field in saccade initiation: executive, not direct, control. Journal Neurophysiology, 103, 801–816.

    Article  PubMed  Google Scholar 

  • Tanaka, M. (2007). Cognitive signals in the primate motor thalamus predict saccade timing. Journal of Neuroscience, 27, 12109–12118.

    Article  CAS  PubMed  Google Scholar 

  • Thakkar, K. N., Schall, J. D., Boucher, L., Logan, G. D., & Park, S. (2011). Response inhibition and response monitoring in a saccadic countermanding task in schizophrenia. Biological Psychiatry, 69, 55–62.

    Article  PubMed  Google Scholar 

  • Thura, D., & Cisek, P. (2016). Modulation of premotor and primary motor cortical activity during volitional adjustments of speed-accuracy trade-offs. Journal of Neuroscience, 36, 938–956.

    Article  CAS  PubMed  Google Scholar 

  • Thura, D., Beauregard-Racine, J., Fradet, C. W., & Cisek, P. (2012). Decision making by urgency gating: theory and experimental support. Journal of Neurophysiology, 108, 2912-2930.

  • Wang, N., Perkins, E., Zhou, L., Warren, S., & May, P. J. (2013). Anatomical evidence that the superior colliculus controls saccades through central mesencephalic reticular formation gating of omnipause neuron activity. Journal of Neuroscience, 9, 16285–16296.

    Article  CAS  Google Scholar 

  • Van Horn, M. R., & Cullen, K. E. (2012). Coding of microsaccades in three-dimensional space by premotor saccadic neurons. Journal of Neuroscience, 32, 1974–1980.

    Article  PubMed  CAS  Google Scholar 

  • Van Horn, M. R., Mitchell, D. E., Massot, C., & Cullen, K. E. (2010). Local neural processing and the generation of dynamic motor commands within the saccadic premotor network. Journal of Neuroscience, 30, 10905-10917.

  • Woodman, G. F., Kang, M. S., Thompson, K., & Schall, J. D. (2008). The effect of visual search efficiency on response preparation: neurophysiological evidence for discrete flow. Psychological science, 19, 128-136.

  • Yoshida, K., Iwamoto, Y., Chimoto, S., & Shimazu, H. (1999). Saccade-related inhibitory input to pontine omnipause neurons: an intracellular study in alert cats. Journal of Neurophysiology, 82, 1198–1208.

    Article  CAS  PubMed  Google Scholar 

  • Zandbelt, B., Purcell, B. A., Palmeri, T. J., Logan, G. D., & Schall, J. D. (2014). Response times from ensembles of accumulators. Proceedings of the National Academy of Sciences USA, 111, 2848–2853.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the many colleagues whose creative and insightful work was reviewed and apologize to those whose work was not highlighted enough or at all owing to limits of space or knowledge.

Funding

MP is supported by the Canadian Institutes of Health Research and the Natural Sciences and Engineering Research Council of Canada. JDS was supported by the National Institutes of Health and by Robin and Richard Patton through the E. Bronson Ingram Chair in Neuroscience.

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Authors and Affiliations

  1. Centre for Vision Research, Vision Science to Application, Department of Biology, York University, Ontario, M3J 1P3, Toronto, Canada

    Jeffrey D. Schall

  2. Department of Biomedical & Molecular Sciences and of Psychology, Queen’s University, Ontario, ON K7L 3N6, Kingston, Canada

    Martin Paré

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All experimental procedures performed in JDS laboratory are in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals, the Society for Neuroscience Guidelines and Policies, and approved by the Vanderbilt University Institutional Animal Care and Use Committee. All experimental procedures performed in MP laboratory are in accordance with the Canadian Council on Animal Care in science and approved by Queen’s University Animal Care Committee. 

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The authors declare no conflict of interest.

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This article belongs to the Topical Collection: Vision and Action Guest Editors: Aasef Shaikh and Jeffrey Shall

Action Editor: Barry Richmond

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Schall, J.D., Paré, M. The unknown but knowable relationship between Presaccadic Accumulation of activity and Saccade initiation. J Comput Neurosci 49, 213–228 (2021). https://doi.org/10.1007/s10827-021-00784-7

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