Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics

Excitatory and inhibitory frequency response areas of 130 neurons of the central nucleus of the mouse inferior colliculus (ICC) were mapped by extracellular single-unit recordings and quantitatively evaluated with regard to thresholds, steepness of slopes of excitatory tuning, characteristic frequencies of excitation (CF(E)), inhibition (CFI), and bandwidths of response areas (sharpness of tuning). Two-tone stimuli were used to determine the shapes of inhibitory response areas. Class I neurons (n=54) had asymmetrical (with regard to the CF(E)) excitatory and inhibitory response areas, with inhibition above CF(E) having lower thresholds and covering larger areas than inhibition below CF(E). Quantitative relationships between CF(E) and CF(I) thresholds, and sharpness of tuning showed that the receptive fields of about two-thirds of these neurons had properties similar to auditory nerve fibers. Class II neurons (n=36) had small symmetrical or tilted excitatory areas of rather constant bandwidths and broad inhibitory areas reaching far into and often through the excitatory area, leading to closed excitatory areas in ten neurons. Class III neurons (n=32) had higher excitatory thresholds and the highest proportions of unilateral inhibitory areas compared with neurons of the other classes. Their excitatory area often widened symmetrically with increasing sound level. Their inhibitory areas did not overlap with the excitatory area. Class IV neurons (n=8) had two branches of excitatory areas (two-CFs(E)) and six of the neurons had a central inhibitory area in addition to the low- and high-frequency inhibitory areas. In most neurons, the shapes of excitatory response areas predicted the shapes of inhibitory areas. Altogether, 15 neurons from all 4 classes had areas of facilitation in addition to inhibitory areas. Facilitation in six class IV neurons occurred between the two branches of the excitatory area. All 130 neurons had large inhibitory areas, 106 of them on both sides of the excitatory area. That is, sound processing in the ICC shows strong inhibitory components. The close relationships between excitatory and inhibitory CFs found here indicate that inhibitory projections to and interactions within the ICC are tonotopically organized comparable to the excitatory ones.