Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. 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 synchronize or phase-lock to low-frequency tones and transmit this temporal information to cells in the anteroventral cochlear nucleus (AVCN). Phase-locking in the AVCN is usually reported to be similar to or weaker than 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 surprise, 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 micropipettes or metal microelectrodes. A series of short tone bursts at increasing sound pressure level (SPL) was presented at the characteristic frequency (CF) of the fiber and phase-locking was quantified with the vector strength R at each SPL. For each fiber the maximum R value (Rmax) was then determined. 3. Low-frequency fibers in the TB showed very precise phase-locking: Rmax values could approach 0.99. For the majority of fibers (33/44, 75%) with CF < 700 Hz, Rmax was > or = 0.9 and therefore higher than is ever observed in the AN. We define such fibers as "high-sync." Most of these fibers also entrained to the stimulus, i.e., they fired a precisely timed action potential to almost every stimulus cycle. Some fibers showed perfect entrainment, with maximum discharge rates equaling the stimulus frequency. 4. To exclude the possibility that stimulus paradigms or acoustic and recording equipment were the source of this enhancement, we obtained additional data on low-frequency AN fibers using the same experimental protocol as in our TB experiments. These AN data agree well with published reports. 5. The morphological class of some of the cells studied was identified on the basis of anatomic features revealed by intra-axonal injection of HRP or Neurobiotin. Labeled low-CF axons (N = 7), which were all high-sync, originated from AVCN bushy cells: five were globular and two were spherical bushy cell axons. 6. Spontaneous rate of high-sync fibers covered a range from 0 to 176 spikes/s but were biased toward low values (mean 16 spikes/s). Responses to broadband clicks and sinusoidally amplitude-modulated signals provided additional evidence of improved timing properties.(ABSTRACT TRUNCATED AT 400 WORDS)