We examined the effect of chronic afferent deprivation on an identified interneuron (Int-i) in the auditory system of the Australian field cricket Teleogryllus oceanicus. In normal intact crickets, the auditory afferents from each ear terminate ipsilaterally onto a single Int-i. Each bilaterally paired Int-i is excited by ultrasound stimulation of its ipsilateral ear but not by the contralateral ear. Unilateral removal of an ear early in postembryonic development deprives the developing Int-i of ipsilateral auditory innervation. Consequently, the ipsilateral dendrites of the deprived interneuron sprout, grow aberrantly across the ganglionic midline, and terminate specifically in the intact auditory neuropile of the contralateral (unlesioned) side, where they form functional synapses with the contralateral afferents. This unusual compensatory dendritic sprouting restores auditory function to the neuron. Thus, it is demonstrated that the dendritic shape of an identified Int, as well as its synaptic connectivity, is altered as a consequence of chronic sensory deprivation.The ability of a neuron to restore its structure and function after lesions have been inflicted on nervous tissue is a fundamental form of neuronal plasticity. Lesions made directly on a neuron by cutting or crushing its axon interrupt a cell's anatomical integrity as well as its physiological functions. However, the neuron may regenerate and thereby restore some measure of structural and functional integrity. A more subtle lesion occurs when a neuron is deprived of its synaptic input even though the neuron is not itself directly damaged. For example, a developing sensory organ can be removed before it makes synapses with target neurons in the central nervous system, effectively deafferenting the latter. Since the morphological targets of afferent terminals are usually the dendrites of the target cell, research has focused on the effect of deafferentation on the dendritic tree of the deprived target neurons. Depending on the species, the target neurons, and the timing ofdeafferentation, the morphological response of the affected dendrites varies from degeneration to no apparent change, to aberrant sprouting; in general, degeneration is more common. In this paper, we describe the effect of deafferentation in the auditory system of the Australian field cricket Teleogryllus oceanicus. We show that an identified auditory interneuron (Int-1) responds to chronic unilateral deafferentation by expanding its dendritic tree into the unlesioned contralateral auditory neuropile and making novel synaptic connections that effectively reafferent the lesioned Int-i, restoring physiological function; some of these results were reported in abstracts (1, 2).The auditory system of T. oceanicus is relatively simple (3,4). The auditory organ is located on the tibial segment of each foreleg. From there, the -"70 axons of the receptor cells run within the leg nerve and terminate in the prothoracic ganglion in a localized region of neuropile (auditory neuropile); ...