The olivocochlear (OC) efferent innervation of the mammalian inner ear consists of two subdivisions, medial (MOC) and lateral (LOC), with different peripheral terminations on outer hair cells and cochlear afferent terminals, respectively. The cochlear effects of electrically activating MOC efferents are well known, i.e., response suppression effected by reducing outer hair cells' contribution to cochlear amplification. LOC peripheral effects are unknown, because their unmyelinated axons are difficult to electrically stimulate. Here, stimulating electrodes are placed in the inferior colliculus (IC) to indirectly activate the LOC system, while recording cochlear responses bilaterally from anesthetized guinea pigs. Shocks at some IC sites produced novel cochlear effects attributable to activation of the LOC system: long-lasting (5-20 min) enhancement or suppression of cochlear neural responses (compound action potentials and round window noise), without changes in cochlear responses dominated by outer hair cells (otoacoustic emissions and cochlear microphonics). These novel effects also differed from classic MOC effects in their lack of dependence on the level and frequency of the acoustic stimulus. These effects disappeared on sectioning the entire OC bundle, but not after selective lesioning of the MOC tracts or the cochlea's autonomic innervation. We conclude that the LOC pathway comprises two functional subdivisions, capable of inducing slow increases or decreases in response magnitudes in the auditory nerve. Such a system may be useful in maintaining accurate binaural comparisons necessary for sound localization in the face of slow changes in interaural sensitivity.