The optic chiasm: a turning point in the evolution of eye/hand coordination.

Abstract

The primate visual system has a uniquely high proportion of ipsilateral retinal projections, retinal ganglial cells that do not cross the midline in the optic chiasm. The general assumption is that this developed due to the selective advantage of accurate depth perception through stereopsis. Here, the hypothesis that the need for accurate eye-forelimb coordination substantially influenced the evolution of the primate visual system is presented. Evolutionary processes may change the direction of retinal ganglial cells. Crossing, or non-crossing, in the optic chiasm determines which hemisphere receives visual feedback in reaching tasks. Each hemisphere receives little tactile and proprioceptive information about the ipsilateral hand. The eye-forelimb hypothesis proposes that abundant ipsilateral retinal projections developed in the primate brain to synthesize, in a single hemisphere, visual, tactile, proprioceptive, and motor information about a given hand, and that this improved eye-hand coordination and optimized the size of the brain. If accurate eye-hand coordination was a major factor in the evolution of stereopsis, stereopsis is likely to be highly developed for activity in the area where the hands most often operate.The primate visual system is ideally suited for tasks within arm’s length and in the inferior visual field, where most manual activity takes place. Altering of ocular dominance in reaching tasks, reduced cross-modal cuing effects when arms are crossed, response of neurons in the primary motor cortex to viewed actions of a hand, multimodal neuron response to tactile as well as visual events, and extensive use of multimodal sensory information in reaching maneuvers support the premise that benefits of accurate limb control influenced the evolution of the primate visual system. The eye-forelimb hypothesis implies that evolutionary change toward hemidecussation in the optic chiasm provided parsimonious neural pathways in animals developing frontal vision and visually guided forelimbs, and also suggests a new perspective on vision convergence in prey and predatory animals.