Recent studies, conducted almost exclusively in primates, have shown that several cortical areas usually associated with modality-specific sensory processing are subject to influences from other senses. Here we demonstrate using single-unit recordings and estimates of mutual information that visual stimuli can influence the activity of units in the auditory cortex of anesthetized ferrets. In many cases, these units were also acoustically responsive and frequently transmitted more information in their spike discharge patterns in response to paired visual–auditory stimulation than when either modality was presented by itself. For each stimulus, this information was conveyed by a combination of spike count and spike timing. Even in primary auditory areas (primary auditory cortex [A1] and anterior auditory field [AAF]), ∼15% of recorded units were found to have nonauditory input. This proportion increased in the higher level fields that lie ventral to A1/AAF and was highest in the anterior ventral field, where nearly 50% of the units were found to be responsive to visual stimuli only and a further quarter to both visual and auditory stimuli. Within each field, the pure-tone response properties of neurons sensitive to visual stimuli did not differ in any systematic way from those of visually unresponsive neurons. Neural tracer injections revealed direct inputs from visual cortex into auditory cortex, indicating a potential source of origin for the visual responses. Primary visual cortex projects sparsely to A1, whereas higher visual areas innervate auditory areas in a field-specific manner. These data indicate that multisensory convergence and integration are features common to all auditory cortical areas but are especially prevalent in higher areas.

Descending corticofugal projections are thought to play a critical role in shaping the responses of subcortical neurons. Here, we examine the origins and targets of ferret auditory corticocollicular projections. We show that the ectosylvian gyrus (EG), where the auditory cortex is located, can be subdivided into middle, anterior, and posterior regions according to the pattern of cytochrome oxidase staining and immunoreactivity for the neurofilament antibody SMI₃₂. Injection of retrograde tracers in the inferior colliculus (IC) labeled large layer V pyramidal cells throughout the EG and adjacent sulci. Each region of the EG has a different pattern of descending projections. Neurons in the primary auditory fields in the middle EG project to the lateral nucleus (LN) of the ipsilateral IC and bilaterally to the dorsal cortex and dorsal part of the central nucleus (CN). The projection to these dorsomedial regions of the IC is predominantly ipsilateral and topographically organized. The secondary cortical fields in the posterior EG target the same midbrain areas but exclude the CN of the IC. A smaller projection to the ipsilateral LN also arises from the anterior EG, which is the only region of auditory cortex to target tegmental areas surrounding the IC, including the superior colliculus, periaqueductal gray, intercollicular tegmentum, and cuneiform nucleus. This pattern of corticocollicular connectivity is consistent with regional differences in physiological properties and provides another basis for subdividing ferret auditory cortex into functionally distinct areas.

In addition to their ascending pathways that originate at the receptor cells, all sensory systems are characterized by extensive descending projections. Although the size of these connections often outweighs those that carry information in the ascending auditory pathway, we still have a relatively poor understanding of the role they play in sensory processing. In the auditory system one of the main corticofugal projections links layer V pyramidal neurons with the inferior colliculus (IC) in the midbrain. All auditory cortical fields contribute to this projection, with the primary areas providing the largest outputs to the IC. In addition to medium and large pyramidal cells in layer V, a variety of cell types in layer VI make a small contribution to the ipsilateral corticocollicular projection. Cortical neurons innervate the three IC subdivisions bilaterally, although the contralateral projection is relatively small. The dorsal and lateral cortices of the IC are the principal targets of corticocollicular axons, but input to the central nucleus has also been described in some studies and is distinctive in its laminar topographic organization. Focal electrical stimulation and inactivation studies have shown that the auditory cortex can modify almost every aspect of the response properties of IC neurons, including their sensitivity to sound frequency, intensity and location. Along with other descending pathways in the auditory system, the corticocollicular projection appears to continually modulate the processing of acoustical signals at subcortical levels. In particular, there is growing evidence that these circuits play a critical role in the plasticity of neural processing that underlies the effects of learning and experience on auditory perception by enabling changes in cortical response properties to spread to subcortical nuclei.