We studied the cytoarchitecture, neurochemical organization, and connections of the sagulum. The goal was to clarify its role in midbrain, lateral tegmental, and thalamic auditory processing. On cytoarchitectonic grounds, ventrolateral (parvocellular) and dorsomedial (magnocellular) subdivisions were recognized. The patterns of immunostaining for gamma-aminobutyric acid (GABA) and glycine were distinct. Approximately 5-10% of the neurons were GABAergic, and more than one type was identified; GABAergic axon terminals were abundant in number and varied in form. Glycinergic neurons were much rarer, < 1% of the population, and glycinergic axon terminals were correspondingly sparse. Wheat germ agglutinin conjugated to horseradish peroxidase was used for purposes of connectional mapping, and biotinylated dextran amines revealed the structure of corticosagular axons. All nine cortical areas injected project to the ipsilateral sagulum. Five (areas AI, AII, SF, EPD, and Te) had heavier projections than the others. Areas AI and AII projected throughout the rostrocaudal sagulum. Labeling from AI was moderate in density and concentrated in the central sagulum, whereas the input from AII was heavier and ended more laterally. Suprasylvian fringe input was light, especially caudally, and was chiefly in the central sagulum. The projection from the dorsal region of the posterior ectosylvian gyrus was comparatively stronger and was in the dorsolateral sagulum. Finally, the temporal cortex sent axons to the most lateral sagulum, spanning the dorsoventral extent, whereas insular cortex axons ended diffusely in the dorsolateral sagulum. Corticofugal axons ranged from fine boutons en passant to larger globular terminals. The sagulum may represent the earliest significant opportunity in the ascending auditory pathway for corticofugal modulation. The most extensive input arises from the polymodal association areas. The sagulum then projects divergently to the dorsal cortex of the inferior colliculus and the dorsal division of the medial geniculate body. The projection from the dorsal division of the auditory thalamus to nonprimary auditory cortex completes this circuit between the forebrain and the midbrain and represents a nexus in the ascending and descending auditory systems. Such circuits could play a critical role in auditory-motor adjustments to sound.