Sounds and beyond: multisensory and other non-auditory signals in the inferior colliculus

The inferior colliculus (IC) is a major processing center situated mid-way along both the ascending and descending auditory pathways of the brain stem. Although it is fundamentally an auditory area, the IC also receives anatomical input from non-auditory sources. Neurophysiological studies corroborate that non-auditory stimuli can modulate auditory processing in the IC and even elicit responses independent of coincident auditory stimulation. In this article, we review anatomical and physiological evidence for multisensory and other non-auditory processing in the IC. Specifically, the contributions of signals related to vision, eye movements and position, somatosensation, and behavioral context to neural activity in the IC will be described. These signals are potentially important for localizing sound sources, attending to salient stimuli, distinguishing environmental from self-generated sounds, and perceiving and generating communication sounds. They suggest that the IC should be thought of as a node in a highly interconnected sensory, motor, and cognitive network dedicated to synthesizing a higher-order auditory percept rather than simply reporting patterns of air pressure detected by the cochlea. We highlight some of the potential pitfalls that can arise from experimental manipulations that may disrupt the normal function of this network, such as the use of anesthesia or the severing of connections from cortical structures that project to the IC. Finally, we note that the presence of these signals in the IC has implications for our understanding not just of the IC but also of the multitude of other regions within and beyond the auditory system that are dependent on signals that pass through the IC. Whatever the IC "hears" would seem to be passed both "upward" to thalamus and thence to auditory cortex and beyond, as well as "downward" via centrifugal connections to earlier areas of the auditory pathway such as the cochlear nucleus.