Anomalous retinal correspondence: Neuroanatomic mechanism in strabismic monkeys and clinical findings in strabismic children

Background: Anomalous retinal correspondence IARC) is a neural adaptation t o eye misalignment in which noncorresponding retinal points are linked in t he visual cortex to provide binocular fusion. ARC within the striate cortex would require that horizontal neurons link right-eye and left-eye ocular d ominance columns (ODCs) separated by a distance in the cortex proportional to the angle of strabismus. Two hypothetical mechanisms are possible: (1) T he ODCs can be linked by axons of horizontal neurons that project monosynap tically from a right-eye to a left-eye ODC. The further apart the ODCs, the longer the axons; hence, axon length should be greater in subjects with st rabismus than in healthy subjects (elongated axon, monosynaptic hypothesis) . In this case, the clinical probability of developing ARC should be indepe ndent of the angle of strabismus, until an upper-limit angle of strabismus is reached equally to the maximal length of axons available to link nonadja cent OD Ca, at which point an abrupt decline of ARC probability should be e vident. (2) Alternatively, ODCs can be linked by a chain of horizontal neur ons, the number of which increases as the distance among ODCs increases; ax on length in subjects with strabismus would be expected to be the same as i n healthy subjects (normal axon, polysynaptic hypothesis). In this case, th e greater the angle of strabismus, the more horizontal neurons and synapses required for linkage, and the greater the probability of signal degradatio n. Thus, the clinical probability of developing ARC through a polysynaptic mechanism should be inversely proportional to the angle of strabismus. The purpose of this study was to test these 2 hypotheses neuroanatomically in p rimates and clinically in children. Methods: For the neuroanatomic portion of the study, biotinylated dextran amine was injected into OD Ca of a rea V 1 to label individual neurons. The length of the horizontal axons from thes e neurons was then compared in strabismic and normal monkeys. In the clinic al portion of the study, the medical records of 192 children with strabismu s were reviewed retrospectively. The angle of strabismus (prism cover test) and the presence of ARC (Bagolini striated lenses, Worth/Polaroid 4-dot) w ere recorded. Plots of the presence of ARC as a function of the angle of st rabismus were obtained. Results: There was no significant difference in axo n length between healthy (7.02 +/- 0.83 mm) and strabismic monkeys (6.60 +/ - 1.07 mm) (P = .16). In children with strabismus, ARC decreased as the ang le of strabismus increased (P < .05). ARC was more prevalent in children wh o had primary or postsurgical deviations of less than or equal to 4 degrees to 5 degrees (8-10 PD), corresponding to less than or equal to 2 horizonta l axon lengths in the foveal striate visual cortex. Conclusions: The visual cortex adapts to strabismus by combining information from paired ODCs of o pposite ocularity that, because of the eye misalignment, are nonadjacent an d separated by abnormally long distances across the striate cortex. The cor tex appears to achieve the linkage, not by elongating neuronal axons, but b y using chains of neurons that have normal-length axons. The visual cortex is most successful stochastically at achieving this linkage tie, developing ARC) when the gap that must be bridged is no greater than 4 degrees to 5 d egrees (8-10 PD), or the retinotopic distance in the foveal visual field is spanned by 2 normal V1 neurons.