The mammalian cochlear nucleus (CN) has been a model structure to study the relationship between physiological and morphological cell classes. Several issues remain, in particular with regard to the projection patterns and physiology of neurons that exit the CN dorsally via the dorsal (DAS), intermediate (IAS), and commissural stria. We studied these neurons physiologically and anatomically using the intra-axonal labeling method. Multipolar cells with onset chopper (OC) responses innervated the ipsilateral ventral and dorsal CN before exiting the CN via the commissural stria. Upon reaching the midline they turned caudally to innervate the opposite CN. No collaterals were seen innervating any olivary complex nuclei. Octopus cells typically showed onset responses with little or no sustained activity. The main axon used the IAS and followed one of two routes occasionally giving off olivary complex collaterals on their way to the contralateral ventral nucleus of the lateral lemniscus (VNLL). Here they can have elaborate terminal arbors that surround VNLL cells. Fusiform and giant cells have overlapping but not identical physiology. Fusiform but not giant cells typically show pauser or buildup responses. Axons of both cells exit via the DAS and take the same course to reach the contralateral IC without giving off any collaterals en route. J. Comp. Neurol. 482:349–371, 2005. © 2005 Wiley-Liss, Inc.