A functional map of the pigeon basilar papilla: correlation of the properties of single auditory nerve fibres and their peripheral origin.

The purpose of the investigation was to correlate the functional properties of primary auditory fibres with the location of appertaining receptor cells in the avian basilar papilla. The functional properties of 425 single afferent fibres from the auditory nerve of adult pigeons were measured. The peripheral innervation site of 39 fibres was identified by intracellular labelling and correlated with the fibre's functional properties. Mean spontaneous firing rate (SR, 0.1-250/s) was distributed monomodally (mean: 91 +/- 47/s) but not normally. Characteristic frequencies (CFs) were in the range of 0.02-4 kHz. SR, threshold at CF (4-76 dB SPL) and sharpness of tuning (Q10 dB, 0.1-8.8) varied systematically with CF. For a given CF there was a strong correlation of threshold and Q10 dB and of threshold and SR. Labelled fibres innervated different hair cell types over 93% of the length and 97% of the width of the basilar papilla. The majority of fibres innervated hair cells located between 30 and 70% distance from the apex and 0 and 30% distance from the neural edge of the papilla. CFs are mapped tonotopically from high at the base to low at the apex of the papilla, with a mean mapping constant of 0.63 +/- 0.05 mm/octave (in vivo). The highest CF at the base extrapolates to 5.98 +/- 1.17 kHz. The lowest CF mapped at the apex is 0.021 kHz. From the data, together with data from mechanical measurements (Gummer et al., 1987), a frequency-place function of the pigeon papilla was calculated. Transverse gradients of threshold at CF and of Q10 dB were observed across the width of the papilla. Thresholds were lowest and sharpness of tuning was highest above the neural limbus at a distance of 23% from the neural edge of the papilla. Hair cells in this sensitive strip are the tallest and narrowest ones across the width of the papilla. They are packed most densely and receive the largest number of afferent fibres. Fibres innervating (mostly short) hair cells on the free basilar membrane were spontaneously active and responsive to sound. Their Q10 dB was less than average but their sensitivity and SR were comparable to the mean population values. It is concluded that functional properties change gradually not only along the length but also across the width of the pigeon basilar papilla. The results support the idea that sharp frequency tuning of avian primary auditory fibres involves tuning mechanisms supplementary to the tuning of the free part of the basilar membrane.