Orienting Gaze Toward a Visual Target: Neurophysiological Synthesis with Epistemological Considerations

Overview

Journal Vision (Basel)

Date 2025 Jan 23

PMID 39846622

Authors

Laurent Goffart

Affiliations

Soon will be listed here.

Abstract

The appearance of an object triggers an orienting gaze movement toward its location. The movement consists of a rapid rotation of the eyes, the saccade, which is accompanied by a head rotation if the target eccentricity exceeds the oculomotor range and by a slow eye movement if the target moves. Completing a previous report, we explain the numerous points that lead to questioning the validity of a one-to-one correspondence relation between measured physical values of gaze or head orientation and neuronal activity. Comparing the sole kinematic (or dynamic) numerical values with neurophysiological recordings carries the risk of believing that the activity of central neurons directly encodes gaze or head physical orientation rather than mediating changes in extraocular and neck muscle contraction, not to mention possible changes happening elsewhere (in posture, in the autonomous nervous system and more centrally). Rather than reducing mismatches between extrinsic physical parameters (such as position or velocity errors), eye and head movements are behavioral expressions of intrinsic processes that restore a poly-equilibrium, i.e., balances of activities opposing antagonistic visuomotor channels. Past results obtained in cats and monkeys left a treasure of data allowing a synthesis, which illustrates the formidable complexity underlying the small changes in the orientations of the eyes and head. The aim of this synthesis is to serve as a new guide for further investigations or for comparison with other species.

References

Barash S, Melikyan A, Sivakov A, Tauber M . Shift of visual fixation dependent on background illumination. J Neurophysiol. 1998; 79(5):2766-81. DOI: 10.1152/jn.1998.79.5.2766. View

Salman M, Sharpe J, Eizenman M, Lillakas L, Westall C, To T . Saccades in children. Vision Res. 2005; 46(8-9):1432-9. DOI: 10.1016/j.visres.2005.06.011. View

Chubb M, Fuchs A . Contribution of y group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements. J Neurophysiol. 1982; 48(1):75-99. DOI: 10.1152/jn.1982.48.1.75. View

Keller E, Gandhi N, Sekaran S . Activity in deep intermediate layer collicular neurons during interrupted saccades. Exp Brain Res. 2000; 130(2):227-37. DOI: 10.1007/s002219900239. View

Takahashi M, Sugiuchi Y, Shinoda Y . Convergent synaptic inputs from the caudal fastigial nucleus and the superior colliculus onto pontine and pontomedullary reticulospinal neurons. J Neurophysiol. 2013; 111(4):849-67. DOI: 10.1152/jn.00634.2013. View

Lynch J, McLAREN J . Deficits of visual attention and saccadic eye movements after lesions of parietooccipital cortex in monkeys. J Neurophysiol. 1989; 61(1):74-90. DOI: 10.1152/jn.1989.61.1.74. View

Appell P, Behan M . Sources of subcortical GABAergic projections to the superior colliculus in the cat. J Comp Neurol. 1990; 302(1):143-58. DOI: 10.1002/cne.903020111. View

Soetedjo R, Kaneko C, Fuchs A . Evidence against a moving hill in the superior colliculus during saccadic eye movements in the monkey. J Neurophysiol. 2002; 87(6):2778-89. DOI: 10.1152/jn.2002.87.6.2778. View

Helmchen C, Straube A, Buttner U . Saccade-related activity in the fastigial oculomotor region of the macaque monkey during spontaneous eye movements in light and darkness. Exp Brain Res. 1994; 98(3):474-82. DOI: 10.1007/BF00233984. View

10.

Fukushima K, Peterson B, Uchino Y, Coulter J, Wilson V . Direct fastigiospinal fibers in the cat. Brain Res. 1977; 126(3):538-42. DOI: 10.1016/0006-8993(77)90604-7. View

11.

ROBINSON F, Fuchs A . The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci. 2001; 24:981-1004. DOI: 10.1146/annurev.neuro.24.1.981. View

12.

Tomlinson R, Robinson D . Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol. 1984; 51(6):1121-36. DOI: 10.1152/jn.1984.51.6.1121. View

13.

Goffart L, Cecala A, Gandhi N . The superior colliculus and the steering of saccades toward a moving visual target. J Neurophysiol. 2017; 118(5):2890-2901. PMC: 5680352. DOI: 10.1152/jn.00506.2017. View

14.

Hanson M, Hamid M, Tomsak R, Chou S, Leigh R . Selective saccadic palsy caused by pontine lesions: clinical, physiological, and pathological correlations. Ann Neurol. 1986; 20(2):209-17. DOI: 10.1002/ana.410200206. View

15.

Wardak C, Olivier E, Duhamel J . Saccadic target selection deficits after lateral intraparietal area inactivation in monkeys. J Neurosci. 2002; 22(22):9877-84. PMC: 6757813. View

16.

Hikosaka O, Igusa Y, Imai H . Inhibitory connections of nystagmus-related reticular burst neurons with neurons in the abducens, prepositus hypoglossi and vestibular nuclei in the cat. Exp Brain Res. 1980; 39(3):301-11. DOI: 10.1007/BF00237119. View

17.

Hafed Z, Goffart L, Krauzlis R . A neural mechanism for microsaccade generation in the primate superior colliculus. Science. 2009; 323(5916):940-3. PMC: 2655118. DOI: 10.1126/science.1166112. View

18.

Goffart L, Pelisson D . Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria. J Neurophysiol. 1998; 79(4):1942-58. DOI: 10.1152/jn.1998.79.4.1942. View

19.

Gottlieb J, Macavoy M, Bruce C . Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J Neurophysiol. 1994; 72(4):1634-53. DOI: 10.1152/jn.1994.72.4.1634. View

20.

Fuchs A, Luschei E . The activity of single trochlear nerve fibers during eye movements in the alert monkey. Exp Brain Res. 1971; 13(1):78-89. DOI: 10.1007/BF00236431. View