ENHANCEMENT OF NEURAL SYNCHRONIZATION IN THE ANTEROVENTRAL COCHLEAR NUCLEUS .2. RESPONSES IN THE TUNING CURVE TAIL

1. Discharges of neurons in the peripheral auditory system contain information about the temporal features of acoustic stimuli. Phase-locking of neurons in the anteroventral cochlear nucleus (AVCN) is usually reported to be less robust than in auditory nerve (AN) fibers, which provide their major input. In a companion paper we reported that some cells in AVCN of the cat show enhanced phase-locking compared with the AN when stimulated at the frequency to which they are most sensitive [characteristic frequency (CF)]. We called neurons ''high-sync'' when they showed vector strengths (R, a measure of phase-locking) greater than or equal to 0.9. Here we report phase-locking properties to stimuli at frequencies below CF. 2. Horseradish peroxidase-filled glass micropipettes or metal microelectrodes were inserted into the trapezoid body (TB), which is the large output tract of the AVCN. Acoustically driven fibers were classified on the basis of the shape of the poststimulus time (PST) histograms to short tone bursts at CF. We then presented low-frequency tones of increasing SPL and determined the maximum R value at 500 Hz (R(500)) for each fiber. Using the same experimental protocol we studied phase-locking in the ANs of two animals because maximal R values at the tuning curve tail have not been reported for AN fibers. 3. Although phase-locking in AN fibers is usually assumed to be independent of CF, we found that fibers with CF >2 kHz tended to have higher R(500) values than fibers with CF less than or equal to 2 kHz. Moreover, R(500) was greater than or equal to 0.9 in 20% (42 of 196) of the fibers studied and could be as high as 0.95. This population of fibers was defined as having ''high-sync tails'' and consisted almost entirely of fibers with low or medium spontaneous rate. 4. High-CF TB fibers stimulated at 500 Hz showed very high phase-locking. High-sync tails (R(500) greater than or equal to 0.9) were found in 41 of 70 TB fibers. For a subset of these fibers (1/3 in total: 23 of 70) phase-locking was higher than is ever observed in the AN (R(500) greater than or equal to 0.95); these fibers were defined as showing synchronization ''enhancement.'' Virtually all fibers showing synchronization enhancement had primary-like-with-notch (PL(N)) PST histograms. Chopper and primary-like fibers showed high-sync tails for CFs >3 kHz. 5. Synchronization filter functions were obtained for high-CF AN fibers by determining maximum synchronization for a range of stimuli below CF. These functions were low-pass, but had higher maximal gain and a lower cutoff frequency than the synchronization function for the population of low-CF AN fibers. These data suggest an apical to basal difference in the cochlear low-pass filtering processes that limits synchronization. 6. Synchronization filter functions of some TB fibers showed enhancement for frequencies <1 kHz, usually accompanied by entrainment. Period histograms at different frequencies, when plotted on the same timescale, were strikingly similar, which suggests that an upper ceiling on phase-locking is set by a constant source of time jitter. In support of this, synchronization filter functions calculated from period histograms obtained at a single fre-quency had a slope that matched the function obtained experimentally.