Functions of the nucleus of the optic tract (NOT). I. Adaptation of the gain of the horizontal vestibulo-ocular reflex

Abstract

We studied the role of the nucleus of the optic tract (NOT) in adapting the gain of the angular vestibulo-ocular reflex (aVOR) in rhesus and cynomolgus monkeys using lesions and temporary inactivation with muscimol. The aVOR gain was adaptively reduced by forced sinusoidal rotation (0.25 Hz, 60 degrees/s) in a self-stationary visual surround, i.e., a visual surround that moved with the subject, or by wearing x0.5 reducing lenses during natural head movements. The aVOR gains dropped by 20-30% after 2 h and by about 30% after 4 h. Muscimol injections caused a loss of adaptation of contraversive-eye velocities induced by the aVOR, and their gains promptly returned to or above preadapted levels. The gains of the adapted ipsiversive and vertical eye velocities produced by the aVOR were unaffected by muscimol injections. Lesions of NOT significantly reduced or abolished the animals' ability to adapt the gain of contraversive aVOR-induced eye velocities, and the monkeys were unable to suppress these contraversive-eye velocities in a self-stationary surround. The lesions did not affect ipsiversive aVOR-induced eye velocities, and the animals were still able to suppress them. Lesions of NOT also affected the unadapted or "default" aVOR gains. After unilateral NOT lesions, gains of ipsiversive aVOR-induced eye velocity were reduced, while gains of contraversive aVOR-induced eye velocity were either unaffected or slightly increased. Consistent with this, muscimol injections into the NOT of unadapted monkeys slightly reduced the gains of ipsiversive and increased the gains of contraversive-eye velocities by about 8-10%. We conclude that each NOT processes ipsiversive retinal-slip information about visual surround movement relative to the head induced by the aVOR. In the presence of visual surround movement, the retinal-slip signal is suppressed, leading to adaptive changes in the gain of aVOR-induced contraversive horizontal eye velocities. NOT also has a role in controlling and maintaining the current state of the aVOR gains. Thus, it plays a unique role in producing and supporting adaptation of the gain of the horizontal aVOR that is likely to be important for stabilizing gaze during head movement. Pathways through the inferior olive are presumably important for this adaptation.