Long-Term Dysfunctions of Neural Stereoscopic Mechanisms After Unilateral Extraocular Muscle Proprioceptive Deafferentation

SUMMARY AND CONCLUSIONS 1. Neural correlates of the permanent deficits in depth perception that occur when extraocular muscle proprioceptive (EMP) afferents are interrupted unilaterally in kittens were investigated by performing extracellular recordings in the primary visual cortex (area 17) in adulthood. Unilateral section of the ophthalmic branch of the trigeminal nerve (V 1 nerve) were performed in 11 cats when they were between 5 and 12 weeks of age (uni-VI group). Electrophysiological results were compared with those obtained in 17 normal adult cats (control group). 2. Binocular interactions were assessed by testing the sensitivity of cortical neurons to dichoptic presentations of moving sinewave gratings whose interocular positional phase relationship was randomly varied. The amplitude modulation between the minimum and the maximum binocular responses defined the dynamic range. The degree of binocular suppression or facilitation was assessed by comparing these binocular response limits with the optimal monocular responses evoked through either eye at the best spatial frequency. The variability of both monocular and binocular responses was estimated by using the variation coefficient. 3. In uni-V 1 cats, both the dynamic range and the degree of binocular suppression were significantly less pronounced than in controls, whereas binocular facilitation was not affected. The variability of the binocular responses was significantly increased, unlike monocular responses, whose variability was similar to control values. 4. From Fourier analysis of the poststimulus time histograms, two clear-cut categories of cells emerged that were differentially affected in the uni-V 1 group. The “modulated” cells showed significantly less binocular suppression than in controls, and the “unmodulated” cells had binocular responses that were significantly more variable than in controls. Results from “simple” cells were similar to those of modulated cells, and results from “complex” cells were similar to those of unmodulated cells. However, in the unmodulated population, which was composed of both simple and complex cells, it was shown that the increase of variability was due to that of complex cells. 5. A nonparametric statistical test was applied on the interocular phase shift tuning curves to determine the minimum stimulus change necessary to elicit a significant change in the neural response. Two categories of cells were determined: the “discriminative” cells (80% in controls but 45% in uni-VI cats) combined pronounced binocular suppression and dynamic range with relatively low variability. The reverse was true in the case of “nondiscriminative” cells (20% in controls and 55% in uni-VI cats). 6. In uni-VI cats, about half of the cells were monocularly activated. However, deficits in binocular discrimination of phase shifts could not be predicted from the ocular dominance breakdown because both monocularly and binocularly activated cells were affected in similar proportions. 7. In uni-V 1 cats, neural binocular discrimination was significantly less affected for cells sensitive to lower spatial frequencies (50.4 cycles per degree) than for cells sensitive to higher spatial frequency ranges. 8. Only cells located in granular and infragranular layers had their neural binocular discrimination affected by the unilateral deafferentation. The effects were particularly strong in cortical layers 4 and 6. 9. The deficits in binocular interactions of area 17 cells correlate with the behavioral deficit in depth perception that occurs when the VI section was performed during the critical period. Balance in proprioceptive inflow is necessary in addition to coherent retinal inputs for the retinal disparity sensitivity of cortical cells to be expressed correctly in adulthood. It is suggested that balanced EMP signals during the critical period are needed to scale and to calibrate binocular retinal disparities to express depth perception.