Voluntary Modulation of Saccadic Peak Velocity Associated with Individual Differences in Motivation

Overview

Journal Cortex

Specialties Neurology
Psychology
Social Sciences

Date 2019 Jan 15

PMID 30638586

Citations 19

Authors

Kinan Muhammed

Edwin Dalmaijer

Sanjay Manohar

Masud Husain

Affiliations

Soon will be listed here.

Abstract

Saccadic peak velocity increases in a stereotyped manner with the amplitude of eye movements. This relationship, known as the main sequence, has classically been considered to be fixed, although several recent studies have demonstrated that velocity can be modulated to some extent by external incentives. However, the ability to voluntarily control saccadic velocity and its association with motivation has yet to be investigated. Here, in three separate experimental paradigms, we measured the effects of incentivisation on saccadic velocity, reaction time and preparatory pupillary changes in 53 young healthy participants. In addition, the ability to voluntarily modulate saccadic velocity with and without incentivisation was assessed. Participants varied in their ability to increase and decrease the velocity of their saccades when instructed to do so. This effect correlated with motivation level across participants, and was further modulated by addition of monetary reward and avoidance of loss. The findings show that a degree of voluntary control of saccadic velocity is possible in some individuals, and that the ability to modulate peak velocity is associated with intrinsic levels of motivation.

Citing Articles

Muscarinic receptors mediate motivation via preparatory neural activity in humans.

Grogan J, Raemaekers M, van Swieten M, Green A, Gillies M, Manohar S Elife. 2024; 13.

PMID: 39565722 PMC: 11578592. DOI: 10.7554/eLife.98922.

Noradrenergic modulation of saccades in Parkinson's disease.

Orlando I, Hezemans F, Ye R, Murley A, Holland N, Regenthal R Brain Commun. 2024; 6(5):fcae297.

PMID: 39464213 PMC: 11503952. DOI: 10.1093/braincomms/fcae297.

Gazing into spatiotemporal 'known unknowns': the influence of uncertainty on pupil size and saccadic eye movements.

Boutachkourt A, Drazyk D, Missal M Sci Rep. 2024; 14(1):17509.

PMID: 39080377 PMC: 11289384. DOI: 10.1038/s41598-024-68233-w.

Motivation by reward jointly improves speed and accuracy, whereas task-relevance and meaningful images do not.

Wolf C, Lappe M Atten Percept Psychophys. 2022; 85(3):930-948.

PMID: 36289140 PMC: 10066132. DOI: 10.3758/s13414-022-02587-z.

Pupil size as a robust marker of attentional bias toward nicotine-related stimuli in smokers.

Blini E, Zorzi M Psychon Bull Rev. 2022; 30(2):596-607.

PMID: 36229711 PMC: 9559544. DOI: 10.3758/s13423-022-02192-z.

References

Takikawa Y, Kawagoe R, Itoh H, Nakahara H, Hikosaka O . Modulation of saccadic eye movements by predicted reward outcome. Exp Brain Res. 2002; 142(2):284-91. DOI: 10.1007/s00221-001-0928-1. View

van Donkelaar P . Eye-hand interactions during goal-directed pointing movements. Neuroreport. 1997; 8(9-10):2139-42. DOI: 10.1097/00001756-199707070-00010. View

Schmidt D, Abel L, DellOsso L, Daroff R . Saccadic velocity characteristics: intrinsic variability and fatigue. Aviat Space Environ Med. 1979; 50(4):393-5. View

Reppert T, Lempert K, Glimcher P, Shadmehr R . Modulation of Saccade Vigor during Value-Based Decision Making. J Neurosci. 2015; 35(46):15369-78. PMC: 4649007. DOI: 10.1523/JNEUROSCI.2621-15.2015. View

Di Stasi L, Antoli A, Canas J . Main sequence: an index for detecting mental workload variation in complex tasks. Appl Ergon. 2011; 42(6):807-13. DOI: 10.1016/j.apergo.2011.01.003. View

Kobayashi S, Nomoto K, Watanabe M, Hikosaka O, Schultz W, Sakagami M . Influences of rewarding and aversive outcomes on activity in macaque lateral prefrontal cortex. Neuron. 2006; 51(6):861-70. DOI: 10.1016/j.neuron.2006.08.031. View

Grace P, Stanford T, Gentgall M, Rolan P . Utility of saccadic eye movement analysis as an objective biomarker to detect the sedative interaction between opioids and sleep deprivation in opioid-naive and opioid-tolerant populations. J Psychopharmacol. 2010; 24(11):1631-40. DOI: 10.1177/0269881109352704. View

Sparks D . The brainstem control of saccadic eye movements. Nat Rev Neurosci. 2002; 3(12):952-64. DOI: 10.1038/nrn986. View

Griffiths B, Beierholm U . Opposing effects of reward and punishment on human vigor. Sci Rep. 2017; 7:42287. PMC: 5304224. DOI: 10.1038/srep42287. View

10.

Tachibana Y, Hikosaka O . The primate ventral pallidum encodes expected reward value and regulates motor action. Neuron. 2012; 76(4):826-37. PMC: 3519929. DOI: 10.1016/j.neuron.2012.09.030. View

11.

Kori A, Miyashita N, Kato M, Hikosaka O, Usui S, Matsumura M . Eye movements in monkeys with local dopamine depletion in the caudate nucleus. II. Deficits in voluntary saccades. J Neurosci. 1995; 15(1 Pt 2):928-41. PMC: 6578280. View

12.

Wang C, Brien D, Munoz D . Pupil size reveals preparatory processes in the generation of pro-saccades and anti-saccades. Eur J Neurosci. 2015; 41(8):1102-10. DOI: 10.1111/ejn.12883. View

13.

Haber S, Knutson B . The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology. 2009; 35(1):4-26. PMC: 3055449. DOI: 10.1038/npp.2009.129. View

14.

Melichar J, Myles J, Eap C, Nutt D . Using saccadic eye movements as objective measures of tolerance in methadone dependent individuals during the hydromorphone challenge test. Addict Biol. 2003; 8(1):59-66. DOI: 10.1080/1355621031000069891. View

15.

Munoz D, Everling S . Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci. 2004; 5(3):218-28. DOI: 10.1038/nrn1345. View

16.

Chen L, Hung L, Quinet J, Kosek K . Cognitive regulation of saccadic velocity by reward prospect. Eur J Neurosci. 2013; 38(3):2434-44. DOI: 10.1111/ejn.12247. View

17.

Manohar S, Husain M . Human ventromedial prefrontal lesions alter incentivisation by reward. Cortex. 2016; 76:104-20. PMC: 4786053. DOI: 10.1016/j.cortex.2016.01.005. View

18.

Snyder L, Calton J, Dickinson A, Lawrence B . Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. J Neurophysiol. 2002; 87(5):2279-86. DOI: 10.1152/jn.00854.2001. View

19.

Ang Y, Lockwood P, Apps M, Muhammed K, Husain M . Distinct Subtypes of Apathy Revealed by the Apathy Motivation Index. PLoS One. 2017; 12(1):e0169938. PMC: 5226790. DOI: 10.1371/journal.pone.0169938. View

20.

Muhammed K, Manohar S, Ben Yehuda M, Chong T, Tofaris G, Lennox G . Reward sensitivity deficits modulated by dopamine are associated with apathy in Parkinson's disease. Brain. 2016; 139(Pt 10):2706-2721. PMC: 5035817. DOI: 10.1093/brain/aww188. View