1. Extracellular single-cell recording techniques were employed to investigate the effects of ocular misalignment on the postnatal development of the spatial response properties of striate cortical neurons. The primary objective of the study was to gain insight into the neural basis of strabismic amblyopia. 2. Two basic rearing strategies were used to study specific aspects of experimental strabismus in developing kittens. In one group, strabismus was optically induced by fitting kittens with goggles that held a 15-diopter base-in prism in front of one eye (MP) or both eyes (BP) between the ages of 4 wk and 4 mo. In the second group, a unilateral esotropia was surgically induced at 3 wks of age either by the simple resection of the lateral rectus muscle tendon (tenotomy) or by a more drastic procedure that involved removing sections of the lateral rectus and superior oblique muscles (myectomy). In addition, the eyelids of the nondeviating eyes of these kittens were sutured closed (ESO/MD). The first rearing paradigm isolated the effects of conflicting visual inputs on neural development, whereas the second procedure isolated the effects of anomalous ocular motility by producing a misalignment without putting the deviated eye at a competitive disadvantage. 3. The recording experiments were conducted when the animals were greater-than-or-equal-to 9 mo of age. A total of 445 striate cortical neurons were isolated and quantitatively studied in 17 cats (3 MPs, 3 BPs, 5 ESO/MDs, 3 goggle-reared controls, and 3 normals). In addition, we analyzed the distribution of preferred stimulus orientations of 1,205 single units that had been studied qualitively in our previous investigation of 42 kittens reared with optically induced strabismus. 4. As expected, the proportion of binocularly driven units was reduced in both MP and BP cats. The great majority of units in ESO/MD animals were exclusively driven or highly dominated by the open deviating eye. 5. Prism-reared animals showed physiological deficits in spatial resolution, contrast sensitivity, contrast gain, and peak firing rate. These effects were manifest in both eyes, although there was always an interocular asymmetry in the deficits observed in the two eyes. In MP animals, the units dominated by the treated eye, which was contralateral to the recording hemisphere, were on the average more severely affected. The interocular asymmetry was smaller in BP cats; however, two of the three BP animals also showed a greater deficit in those units dominated by the contralateral eye. On the other hand, the cells dominated by the contralateral eye in control animals typically exhibited stronger responses than those dominated by the ipsilateral eye. The spatial resolution, contrast sensitivity, contrast gain, and peak firing rate of cortical neurons in all five ESO/MD cats were not significantly different from those in normal control animals. 6. There was a reduced proportion of cortical neurons tuned to vertically oriented contours ("vertical effect") in prism-reared animals. This effect was related to the degree of residual cortical binocularity. However, no measurable differences were found in either the responsiveness or in the degree of orientation selectivity between vertically tuned neurons and units tuned to horizontal stimulus orientations. 7. No differences were noted in any of the response properties examined between ESO/MD cats treated with tenotomy and those treated with myectomy. 8. The data suggest that early disruption of binocularly correlated inputs by itself was sufficient to initiate the neural changes that lead to abnormal spatial properties in cortical neurons in strabismics and that neither altered proprioceptive feedback associated with strabismus surgery nor anomalous ocular mortility per se directly causes the development of abnormal spatial properties. Instead, anomalous binocular interactions in the geniculostriate pathway appear to be the critical factor in the deficits that are observed in strabismic cats.
