A neuroethological theory of the operation of the inferior colliculus.

A general statement of the function of the inferior colliculus is lacking, even after more than three decades of electrophysiological investigation. A neuroethological theory is proposed that accounts for a large and diverse body of evidence. Although aimed at characterizing the inferior colliculus in mammals, the theory also applies generally to the auditory midbrain in vertebrates. The theory has two hypotheses: (1) Tuning processes in the inferior colliculus are related to the biological importance of sounds. (2) There is a change in timing properties at the inferior colliculus, from rapid input to slowed output; this transformation is related to the timing of specific behaviors. Expressed in neuroethological terms, at least some neurons in the inferior colliculus are tuned to sign-stimuli, and the processing of these sign stimuli triggers fixed action patterns for hunting, escape or vocal communication. The resulting temporal transformation adjusts the pace of sensory input to the pace of behavior. Evidence for the theory comes from anatomical, neurophysiological and behavioral studies and includes: (1) massive convergence of parallel auditory pathways at the inferior colliculus, (2) interaction of the inferior colliculus with motor systems, (3) tuning of auditory midbrain neurons to biologically important sounds, (4) the slow pace of neural processing at the inferior colliculus, (5) the slow pace of motor output. The theory has the following implications. Neurons in the inferior colliculus are filters for sounds that require immediate action, such as certain sounds made by prey, predators or conspecifics. Neural processing in the inferior colliculus is species specific, resulting in filtering for these kinds of sounds. Specific action patterns should be correlated with the activity of neurons in the inferior colliculus. Motor activities may modify neural processing in inferior colliculus neurons. The rate at which information is transmitted to the thalamus is regulated by the inferior colliculus.