Binocular maps in Xenopus tectum: Visual experience and the development of isthmotectal topography

Abstract

Xenopus frogs have a prominent binocular field that develops as a consequence of the migration of the eyes during the remodeling of the head during and after metamorphosis. In the optic tectum, a topographic representation of the ipsilateral eye develops during this same period. It is relayed indirectly, via the nucleus isthmi. In the early stages of binocular development, the topographic matching of the ipsilateral input and the retinotectal input from the contralateral eye is largely governed by chemical cues, but the ultimate determinant of the ipsilateral map is binocular visual input. Visual input is such a dominant factor that abnormal visual input resulting from unilateral eye rotation can induce isthmotectal axons to alter their trajectories dramatically, even shifting their terminal zones from one pole of the tectum to the other. This plasticity normally is high only during a 3–4 month critical period of late tadpole-early juvenile life, but the critical period can be extended indefinitely by dark-rearing. NMDA receptors are involved in this process; plasticity can be blocked or promoted by chronic treatment with NMDA antagonists or agonists, respectively. Cholinergic nicotinic receptors on retinotectal axons are likely to play an essential role as well. Modifications in the polysialylation of NCAM are correlated with the state of plasticity. The circuitry underlying binocular plasticity is not yet fully understood but has proved not to be a simple convergence of ipsilateral and contralateral inputs onto the same targets.

Hypothalamic Projections to the Optic Tectum in Larval Zebrafish

“…In teleost fish, tectal afferents arrive in the tectal neuropil, which comprises (from dorsal to ventral): the stratum fibrosum marginale (SM), which does not receive direct retinal inputs, the stratum opticum (SO), stratum fibrosum et griseum superficiale (SFGS), stratum griseum centrale (SGC) and the stratum album centrale and stratum griseum periventriculare (SAC/SPV; Vanegas et al, 1974 ; Meek, 1983 ; Sas and Maler, 1986 ; Meek and Nieuwenhuys, 1998 ). The laminae spanning from the SO to the SAC/SPV are demarcated by robust innervation from the axons of retinal ganglion cells (RGCs), which convey visual information to the tectum (Fiebig et al, 1983 ; Struermer, 1988 ; Streidter and Northcutt, 1989 ; Niell and Smith, 2005 ; Corbo et al, 2012 ; Udin, 2012 ). In contrast, the SM receives axonal projections from the torus longitudinalis (Meek and Schellart, 1978 ; Perry et al, 2010 ), and lacks direct retinal inputs.…”

Direct intertectal inputs are an integral component of the bilateral sensorimotor circuit for behavior in Xenopus tadpoles

“…Together with previous work showing that unilateral tectal injury was sufficient to disrupt avoidance behavior regardless of the side of the approach of a looming stimulus (McKeown et al 2013), this result demonstrates that cutting the intertectal commissure interferes with the tectal function of coordinating bilateral sensory input with motor output. This indicates that the integration of visual information from both eyes is crucial to survival, even at this early developmental stage when adult circuitry for binocular vision has not yet developed (Udin 2012).…”

N-methyl-D-aspartate receptors strongly regulate postsynaptic activity levels during optic nerve regeneration

“…During regeneration, for example, retinal ganglion cells retain their receptive field properties (Oh and Northmore, ) and maintain continuous ongoing activity rather than bursting seen during development (Kolls and Meyer, ). Downstream tectal function, such as tectal output to the nucleus isthmi in frog, is also maintained during optic nerve regeneration (Udin, ). In short, regeneration is a complex amalgam of developmental‐like processes associated with the reestablishment of specific connections and stable neuronal function.…”

“…In the visual system, where this has been most intensely investigated, impulse activity has been shown to mediate the formation of precise retinotopic order in the primary optic projection in a variety of species from frogs to mammals. The formation of a number of other features of the visual pathway such as the laminar innervation of dorsal lateral geniculate, center surround properties of geniculate neurons, ocular dominance columns in visual cortex, alignment of the indirect ipsilateral projection in frog, and a number of response properties of neurons in visual cortex and frog optic tectum have all been shown to be sculpted by impulse activity (Udin and Fawcett, ; Katz and Shatz, ; Ruthazer and Cline, ; Ewald and Cline, ; Udin, ).…”