ENHANCEMENT OF NEURAL SYNCHRONIZATION IN THE ANTEROVENTRAL COCHLEAR NUCLEUS .1. RESPONSES TO TONES AT THE CHARACTERISTIC FREQUENCY

1. Encoding temporal features of the acoustic waveform is an important attribute of the auditory system. Auditory nerve (AN) fibers synchron ize or phase-lock to low-frequency tones and transmit this temporal in formation to cells in the anteroventral cochlear nucleus (AVCN). Phase -locking in the AVCN is usually reported to be similar to or weaker th an in the AN. We studied phase-locking in axons of the trapezoid body (TB), which is the output tract of the AVCN, and found, to our surpris e, that most TB axons exhibited enhanced synchronization compared with AN fibers. 2. Responses from axons in the TB of the cat were obtained with horseradish peroxidase (HRP)- or Neurobiotin-filled micropipette s or metal microelectrodes. A series of short tone bursts at increasin g sound pressure level (SPL) was presented at the characteristic frequ ency (CF) of the fiber and phase-locking was quantified with the vecto r strength R at each SPL. For each fiber the maximum R value (R(max)) was then determined. 3. Low-frequency fibers in the TB showed very pre cise phase-locking: R(max) values could approach 0.99. For the majorit y of fibers (33/44, 75%) with CF <700 Hz, R(max) was greater than or e qual to 0.9 and therefore higher than is ever observed in the AN. We d efine such fibers as ''high-sync.'' Most of these fibers also entraine d to the stimulus, i.e., they fired a precisely timed action potential to almost every stimulus cycle. Some fibers showed perfect entrainmen t, with maximum discharge rates equaling the stimulus frequency. 4. To exclude the possibility that stimulus paradigms or acoustic and recor ding equipment were the source of this enhancement, we obtained additi onal data on low-frequency AN fibers using the same experimental proto col as in our TB experiments. These AN data agree well with published reports. 5. The morphological class of some of the cells studied was i dentified on the basis of anatomic features revealed by intra-axonal i njection of HRP or Neurobiotin. Labeled low-CF axons (N = 7), which we re all high-sync, originated from AVCN bushy cells: five were globular and two were spherical bushy cell axons.6. Spontaneous rate of high-s ync fibers covered a range from 0 to 176 spikes/s but were biased towa rd low values (mean 16 spikes/s). Responses to broadband clicks and si nusoidally amplitude-modulated signals provided additional evidence of improved timing properties. 7. Entrainment and improvement in synchro nization at CF can be generated with a model that incorporates 1) conv ergence of inputs from two or more AN fibers onto an AVCN cell and 2) a postsynaptic cell that requires coincident input spikes before it ge nerates an output spike. The model produces R and average rate values with a realistic dependence on SPL and output discharge patterns that display temporal adaptation. 8. AVCN bushy cells relay signals to bina ural comparison circuits in the brain stem. The sharpening of temporal information observed here may be important for the extraction of inte raural time difference, which is an important cue for sound localizati on.