Neural encoding of single-formant stimuli in the cat. II. Responses of anteroventral cochlear nucleus units

1. We have studied responses of anteroventral cochlear nucleus (AVCN) units to single-formant stimuli (SFS), in an effort to make quantitative comparisons with responses observed in auditory-nerve fibers (ANFs) to the same stimuli (Wang and Sachs 1993) and to reveal some of the signal processing mechanisms at the AVCN. Single-unit recordings and subsequent analyses were performed on each type of commonly recorded units, namely primarylike (Pri), primarylike with notch (PN), sustained chopper (ChS), transient chopper (ChT), and onset chopper (OnC), as well as a few onset (On) units, from the AVCN in anesthetized cats. The responses were obtained at a wide range of sound levels and at a frequency range of 1-10 kHz. Modulation in the envelopes of discharge patterns was quantified by a measure called modulation depth. 2. At moderate to high sound levels, most AVCN units were found to have enhanced modulation depth compared with that of ANFs, although the degree of enhancement varies among different types. All AVCN units, except Pri type, showed an enhancement in modulation depth over that of the highest of ANFs at moderate to high sound levels in the order of (from the highest to the lowest) On, OnC, ChT/PN, and ChS. Specifically, 1) modulation depth in Pri units was comparable to that of high spontaneous rate (SR) ANFs at low sound levels and to that of low/medium SR ANFs at high sound levels (in dB SPL). When sound level was normalized by unit threshold, Pri units, on average, exhibited only limited enhancement in envelope modulation at high sound levels (>80 dB re threshold); 2) PN units showed substantially enhanced modulation depth over that of all SR groups of ANFs at moderate to high sound levels in dB SPL or dB re threshold scales; 3) significant enhancement in modulation depth was seen in both ChS and ChT units, with a slightly higher modulation depth in ChT type across sound levels (in dB SPL or dB re threshold); 4) modulation depth of OnC units was higher than those of primary-like (Pri and PN) and chopper (ChS and ChT) units at a wide range of sound levels; 5) responses from a limited sample of On units showed the highest modulation depth among all types of AVCN units. 3. Detailed analysis revealed that the enhanced modulation depth in the responses of AVCN units is the result of increased envelope peak height and decreased envelope minimum, relative to those of ANFs. In particular, 1) PN units achieved this enhanced modulation depth mainly by a reduction in the envelope minimum and a small increase in the envelope peak height; 2) the enhancement in ChS and ChT units resulted from decreased envelope minimum and substantially increased envelope peak height; 3) the greatly reduced envelope minimum in OnC units is the crucial factor in the observed enhancement. Some of OnC units also showed significantly increased envelope peak height; 4) high modulation depth in On units was caused by an extremely low envelope minimum. Data presented in this study also showed that AVCN units can have different average discharge rates and yet still exhibit enhanced modulation depth. 4. The envelope latency of responses to SFS in AVCN units exhibited properties similar to the first spike latency determined by tonal stimuli. ChS/ChT units were found to have longer latency than Pri/PN units do at all frequencies studied. For both Pri/PN and ChS/ChT units, envelope latency decreased as sound level increased. However, there was a greater reduction in latency from low to high sound level in ChS/ChT units than in Pri/PN units. 5. The results of the present study suggest convergence of multiple ANFs on an AVCN cell as a mechanism for the observed increment in envelope peak height. The effect of convergence is stronger at high sound levels if inputs from low/medium SR or off-best frequency (BF) ANFs are present. Two mechanisms are suggested to explain the reduction in envelope minimum: 1) a threshold effect due to temporal integration of subthreshold excitatory postsynaptic potentials (EPSPs) and 2) somatic inhibition that changes the discharge threshold in an AVCN cell. The above three mechanisms are proposed as potential candidates responsible for the observed modulation enhancement.