Abstract
To test the hypothesis that the premotor cortex in and behind the caudal bank of the arcuate sulcus can generate saccades, we stimulated electrically the periarcuate region of alert rhesus monkeys. We were able to produce saccades from sites of the premotor cortex that were contiguous with the frontal eye fields and extended up to 2 mm behind the smooth pursuit area. However, premotor sites often elicited saccades with ipsiversive characteristic vectors, lower peak velocities, and flatter velocity profiles when compared to saccades evoked from the frontal eye field.
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References
Amiez C, Petrides M (2009) Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Prog Neurobiol 89:220–230. doi:10.1016/j.pneurobio.2009.07.010
Baker JT, Patel GH, Corbetta M, Snyder LH (2006) Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades. Cereb Cortex 16:447–459. doi:10.1093/cercor/bhi124
Borra E, Belmalih A, Gerbella M, Rozzi S, Luppino G (2010) Projections of the hand field of the macaque ventral premotor area F5 to the brainstem and spinal cord. J Comp Neurol 518:2570–2591. doi:10.1002/cne.22353
Borra E, Gerbella M, Rozzi S, Tonelli S, Luppino G (2014) Projections to the superior colliculus from inferior parietal, ventral premotor, and ventrolateral prefrontal areas involved in controlling goal-directed hand actions in the macaque. Cereb Cortex 24:1054–1065. doi:10.1093/cercor/bhs392
Bruce CJ, Goldberg ME, Stanton GB, Bushnell MC (1985) Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J Neurophysiol 54: 714–734. http://jn.physiology.org/content/54/3/714
Chen LL (2006) Head movements evoked by electrical stimulation in the frontal eye field of the monkey: evidence for independent eye and head control. J Neurophysiol 95:3528–3542. doi:10.1152/jn.01320.2005
Cromer JA, Waitzman DM (2006) Neurones associated with saccade metrics in the monkey central mesencephalic reticular formation. J Physiol 570:507–523. doi:10.1113/jphysiol.2005.096834
Distler C, Hoffmann K-P (2015) Direct projections from the dorsal premotor cortex to the superior colliculus in the macaque (Macaca mulatta). J Comp Neurol 523:2390–2408. doi:10.1002/cne.23794
Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77:677–682. doi:10.1016/S0031-9384(02)00929-0
Freedman EG (2001) Interactions between eye and head control signals can account for movement kinematics. Biol Cybern 84:453–462. doi:10.1007/PL00007989
Freedman EG, Sparks DL (1997) Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77: 2328–2348. http://jn.physiology.org/content/77/5/2328
Fries W (1984) Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230:55–76. doi:10.1002/cne.902300106
Fries W (1985) Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey. Behav Brain Res 18:95–105. doi:10.1016/0166-4328(85)90066-X
Fuchs AF (1967) Saccadic and smooth pursuit eye movements in the monkey. J Physiol Lond 191:609–631. doi:10.1113/jphysiol.1967.sp008271
Fujii N, Mushiake H, Tanji J (1998) An oculomotor representation area within the ventral premotor cortex. Proc Natl Acad Sci USA 95:12034–12037. doi:10.1073/pnas.95.20.12034
Fujii N, Mushiake H, Tanji J (2000) Rostrocaudal distinction of the dorsal premotor area based on oculomotor involvement. J Neurophysiol 83: 1764–1769. http://jn.physiology.org/content/83/3/1764.long
Godschalk M, Mitz AR, van Duin B, van der Burg H (1995) Somatotopy of monkey premotor cortex examined with microstimulation. Neurosci Res 23:269–279. doi:10.1016/0168-0102(95)00950-7
Goldberg ME, Bushnell MC, Bruce CJ (1986) The effect of attentive fixation on eye movements evoked by electrical stimulation of the frontal eye fields. Exp Brain Res 61:579–584. doi:10.1007/BF00237584
Goossens HHLM, van Opstal AJ (2000) Blink-perturbed saccades in monkey. I. Behavioral analysis. J Neurophysiol 83: 3411–3429. http://jn.physiology.org/content/83/6/3411.long
Gottlieb JP, Bruce CJ, MacAvoy MG (1993) Smooth eye movements elicited by microstimulation in the primate frontal eye field. J Neurophysiol 69: 786–799. http://jn.physiology.org/content/69/3/786.long
Graziano MSA, Hu XT, Gross CG (1997) Visuospatial properties of ventral premotor cortex. J Neurophysiol 77:2268–2292. http://jn.physiology.org/content/77/5/2268.long
Graziano MSA, Taylor CSR, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851. doi:10.1016/S0896-6273(02)00698-0
Gregoriou GG, Savaki HE (2003) When vision guides movement: a functional imaging study of the monkey brain. Neuroimage 19:959–967. doi:10.1016/S1053-8119(03)00176-9
Huerta MF, Krubitzer LA, Kaas JH (1987) Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkey. II. Cortical connections. J Comp Neurol 265:332–361. doi:10.1002/cne.902650304
Jacobson S, Trojanowski JQ (1977) Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents. Brain Res 132:209–233. doi:10.1016/0006-8993(77)90417-6
Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurements of eye position: an improved method. Vis Res 20:535–538. doi:10.1016/0042-6989(80)90128-5
Kaneko CRS (1996) Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. J Neurophysiol 75: 2229–2242. http://jn.physiology.org/content/75/6/2229.long
Kardamakis A, Grantyn A, Moschovakis AK (2010) Neural network simulations of the primate oculomotor system. V. Eye-head coordination. Biol Cybern 102:209–225. doi:10.1007/s00422-010-0363-0
Knight TA, Fuchs AF (2007) Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation. J Neurophysiol 97:618–634. doi:10.1152/jn.00256.2006
Koyama M, Hasegawa I, Osada T, Adachi Y, Nakahara K, Miyashita Y (2004) Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41:795–807. doi:10.1016/S0896-6273(04)00047-9
Lanciego JL, Luquin MR, Guillén J, Giménez-Amaya JM (1998) Multiple neuroanatomical tracing in primates. Brain Res Protoc 2:323–332. doi:10.1016/S1385-299X(98)00007-5
Leichnetz GR, Spencer RF, Hardy SGP, Astruc J (1981) The prefrontal corticotectal projection in the monkey: an anterograde and retrograde horseradish peroxidase study. Neuroscience 6:1023–1041. doi:10.1016/0306-4522(81)90068-3
Leichnetz GR, Smith DJ, Spencer RF (1984) Cortical projections to paramedian tegmental and basilar pons in the monkey. J Comp Neurol 228:388–408. doi:10.1002/cne.902280307
McIlwain JT (1988) Effects of eye position on electrically evoked saccades: a theoretical note. Vis Neurosci 1:239–244. doi:10.1017/S0952523800001498
Mesulam M-M (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10:309–325. doi:10.1002/ana.410100402
Monteon JA, Constantin AG, Wang H, Martinez-Trujillo J, Crawford JD (2010) Electrical stimulation of the frontal eye fields in the head-free macaque evokes kinematically normal 3D gaze shifts. J Neurophysiol 104:3462–3475. doi:10.1152/jn.01032.2009
Moschovakis AK (1994) Neural network simulations of the primate oculomotor system. I. The vertical saccadic burst generator. Biol Cybern 70:291–302. doi:10.1007/BF00197610
Moschovakis AK, Dalezios Y, Petit J, Grantyn AA (1998) New mechanism that accounts for position sensitivity of saccades evoked in response to electrical stimulation of superior colliculus. J Neurophysiol 80: 3373–3379. http://jn.physiology.org/content/80/6/3373.long
Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W, Guldin W, Hadjidimitrakis K, Savaki HE (2004) Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study. J Neurosci 24:5726–5740. doi:10.1523/JNEUROSCI.1223-04.2004
Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G (1997) Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol 78: 2226–2230. http://jn.physiology.org/content/78/4/2226.long
Neromyliotis E, Moschovakis AK (2016) Involvement of the premotor cortex (Area 6) in saccade generation. In: 10th FENS forum of neuroscience, Kopenhagen, Denmark
Neromyliotis E, Moschovakis AK (2017) Response properties of motor equivalence neurons of the primate premotor cortex. Front Behav Neurosci 11:1–21. doi:10.3389/fnbeh.2017.00061
Papadourakis V, Raos V (2015) Mirror neurons respond to the observation of intransitive actions. In: Soc. for Neurosci., Chicago, IL
Pesaran B, Nelson MJ, Andersen RA (2010) A relative position code for saccades in dorsal premotor cortex. J Neurosci 30:6527–6537. doi:10.1523/JNEUROSCI.1625-09.2010
Raos V, Franchi G, Galesse V, Fagassi L (2003) Somatotopic organization of the lateral part of area F2 (dorsal premotor cortex) of the macaque monkey. J Neurophysiol 89:1503–1518. doi:10.1152/jn.00661.2002
Raos V, Evangeliou MN, Savaki HE (2004) Observation of action: grasping with the mind’s hand. Neuroimage 23:193–201. doi:10.1016/j.neuroimage.2004.04.024
Raos V, Umilta MA, Murata A, Fogassi L, Gallese V (2006) Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. J Neurophysiol 95:709–729. doi:10.1152/jn.00463.2005
Remmel RS (1984) An inexpensive eye movement monitor using the sclera coil technique. IEEE Trans Biomed Eng 4:388–390. doi:10.1109/TBME.1984.325352
Rizzolatti G, Matelli M, Pavesi G (1983) Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106:655–673. doi:10.1093/brain/106.3.655
Rizzolatti G, Camadra R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey: iI. Area F5 and the control of distal movements. Exp Brain Res 71:491–507. doi:10.1007/BF00248742
Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145. doi:10.1109/TBMEL.1963.4322822
Rottach KG, Das VE, Wohlgemuth W, Zivotofsky Z, Leigh RJ (1998) Properties of horizontal saccades accompanied by blinks. J Neurophysiol 79: 2895–2902. http://jn.physiology.org/content/79/6/2895.long
Russo GS, Bruce CJ (1993) Effect of eye position within the orbit on electrically elicited saccadic eye movements: A comparison of the macaque monkey’s frontal and supplementary eye fields. J Neurophysiol 69: 800–818. http://jn.physiology.org/content/69/3/800
Savaki HE, Gregoriou GG, Bakola S, Moschovakis AK (2015) Topography of visuomotor parameters in the frontal and premotor eye fields. Cereb Cortex 25:3095–3106. doi:10.1093/cercor/bhu106
Schultz KP, Williams CR, Busettini C (2010) Macaque pontine omnipause neurons play no direct role in the generation of eye blinks. J Neurophysiol 103:2255–2274. doi:10.1152/jn.01150.2009
Scudder CA, Moschovakis AK, Karabelas AB, Highstein SM (1996) Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons. J Neurophysiol 76: 353–370. http://jn.physiology.org/content/76/1/353.long
Segraves MA, Goldberg ME (1987) Functional properties of corticotectal neurons in the monkey’s frontal eye field. J Neurophysiol 58: 1387–1419. http://jn.physiology.org/content/58/6/1387.long
Stanton GB, Friedman HR, Dias EC, Bruce CJ (2005) Cortical afferents to the smooth-pursuit region of the macaque monkey’s frontal eye field. Exp Brain Res 165:179–192. doi:10.1007/s00221-005-2292-z
Strassman A, Highstein SM, McCrea RA (1986a) Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J Comp Neurol 249:337–357. doi:10.1002/cne.902490303
Strassman A, Highstein SM, McCrea RA (1986b) Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons. J Comp Neurol 249:358–380. doi:10.1002/cne.902490304
Tanaka M, Fukushima K (1998) Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J Neurophysiol 80: 28–47. http://jn.physiology.org/content/80/1/28.long
Wang N, Perkins E, Zhou L, Warren S, May PJ (2017) Reticular formation connections underlying horizontal gaze: the central mesencephalic reticular formation (cMRF) as a conduit for the collicular saccade signal. Front Neuroanat 11:1–20. doi:10.3389/fnana.2017.00036
Acknowledgements
The authors wish to thank V. Raos, G. Gregoriou, and V. Papadourakis for participating in some of the early experiments and A. Tzanou and Y. Dalezios for the histology. The financial support of the Action « Herakleitus II » of the Operational Program “Education and Lifelong Learning” (Action’s Beneficiary: General Secretariat for Research and Technology), co-financed by the European Social Fund (ESF) and Greece, is gratefully acknowledged.
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Neromyliotis, E., Moschovakis, A.K. Saccades evoked in response to electrical stimulation of the posterior bank of the arcuate sulcus. Exp Brain Res 235, 2797–2809 (2017). https://doi.org/10.1007/s00221-017-5012-6
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DOI: https://doi.org/10.1007/s00221-017-5012-6