Self-moved target eye tracking in control and deafferented subjects: roles of arm motor command and proprioception in arm-eye coordination.

1. When a visual target is moved by the subject's hand (self-moved target tracking), smooth pursuit (SP) characteristics differ from eye-alone tracking: SP latency is shorter and maximal eye velocity is higher in self-moved target tracking than in eye-alone tracking. The aim of this study was to determine which signals (motor command and/or proprioception) generated during arm motion are responsible for the decreased time interval between arm and eye motion onsets in self-moved target tracking. 2. Six control subjects tracked a visual target whose motion was generated by active or passive movements of the observer's arm in order to determine the role played by arm proprioception in the arm-eye coordination. In a second experiment, the participation of two subjects suffering complete loss of proprioception allowed us to assess the contribution of arm motor command signals. 3. In control subjects, passive movement of the arm led to eye latencies significantly longer (130 ms) than when the arm was actively self-moved (-5 ms:negative values meaning that the eyes actually started to move before the target) but slightly shorter than in eye-alone tracking (150 ms). These observations indicate that active movement of the arm is necessary to trigger short-latency SP of self-moved targets. 4. Despite the lack of proprioceptive information about arm motion, the two deafferented subjects produced early SP (-8 ms on average) when they actively moved their arms. In this respect they did not differ from control subjects. Active control of the arm is thus sufficient to trigger short-latency SP. However, in contrast with control subjects, in deafferented subjects SP gain declined with increasing target motion frequency more rapidly in self-moved target tracking than in eye-alone tracking. 5. The deafferented subjects also tracked a self-moved target while the relationship between arm and target motions was altered either by introducing a delay between arm motion and target motion or by reversing target motion relative to arm motion. As with control subjects, delayed target motion did not affect SP latency. Furthermore, the deafferented subjects adapted to the reversed arm-target relationship faster than control subjects. 6. The results suggest that arm motor command is necessary for the eye-to-arm motion onset synchronization, because eye tracking of the passively moved arm was performed by control subjects with a latency comparable with that of eye-alone tracking of an external target. On the other hand, as evidenced by the data from the deafferented subjects, afferent information does not appear to be necessary for reducing the time between arm motion and SP onsets. However, afferent information appears to contribute to the parametric adjustment between arm motor command and visual information about arm motion.

[1]  M. Steinbach,et al.  Eye tracking of self-moved targets: the role of efference. , 1969, Journal of experimental psychology.

[2]  I P Howard,et al.  Perceptual learning and adaptation. , 1971, British medical bulletin.

[3]  R W Angel,et al.  Transfer of information from manual to oculomotor control system. , 1972, Journal of experimental psychology.

[4]  James R. Lackner,et al.  Pursuit eye movements elicited by muscle afferent information , 1975, Neuroscience Letters.

[5]  Eileen Kowler,et al.  The effect of expectations on slow oculomotor control—IV. Anticipatory smooth eye movements depend on prior target motions , 1984, Vision Research.

[6]  Otmar Bock,et al.  Coordination of arm and eye movements in tracking of sinusoidally moving targets , 1987, Behavioural Brain Research.

[7]  Harry J. Wyatt,et al.  Smooth eye movements with step-ramp stimuli: The influence of attention and stimulus extent , 1987, Vision Research.

[8]  Eileen Kowler.  Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit , 1989, Vision Research.

[9]  C Ghez,et al.  Roles of proprioceptive input in the programming of arm trajectories. , 1990, Cold Spring Harbor symposia on quantitative biology.

[10]  A. Hough.  Pride and a Daily Marathon , 1992 .

[11]  E. Sedgwick,et al.  The perceptions of force and of movement in a man without large myelinated sensory afferents below the neck. , 1992, The Journal of physiology.

[12]  D Guitton,et al.  Central Organization and Modeling of Eye‐Head Coordination during Orienting Gaze Shifts a , 1992, Annals of the New York Academy of Sciences.

[13]  G M Gauthier,et al.  Dynamic analysis of human visuo-oculo-manual coordination control in target tracking tasks. , 1993, Aviation, space, and environmental medicine.

[14]  Evidence of a limited motor memory for wrist movement in a subject with peripheral neuropathy , 1993 .

[15]  S C Gandevia,et al.  Neural and biomechanical specializations of human thumb muscles revealed by matching weights and grasping objects. , 1993, The Journal of physiology.

[16]  P. van Donkelaar,et al.  Interactions between the eye and hand motor systems: disruptions due to cerebellar dysfunction. , 1994, Journal of neurophysiology.

[17]  C. Bard,et al.  Weight judgment. The discrimination capacity of a deafferented subject. , 1995, Brain : a journal of neurology.

[18]  Y. Lamarre,et al.  Postural adjustments associated with different unloadings of the forearm: effects of proprioceptive and cutaneous afferent deprivation. , 1995, Canadian journal of physiology and pharmacology.

[19]  R. Daroff,et al.  Clinical Neurology for Psychiatrists , 1995, Neurology.

[20]  R. Miall,et al.  Task-dependent changes in visual feedback control: a frequency analysis of human manual tracking. , 1996, Journal of motor behavior.