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Journal of Neuroscience, Vol 3, 2128-2145, Copyright © 1983 by Society for Neuroscience

ARTICLE

Synaptic plasticity within the interpeduncular nucleus after unilateral lesions of the habenula in neonatal rats

GS Hamill and NJ Lenn

In rats, synaptic terminations of the medial habenular (MH) afferents to the interpeduncular nucleus (IPN) are just beginning to form at the time of birth. The alterations in synaptogenesis resulting from unilateral MH lesions placed in neonatal rats were demonstrated with the autoradiographic and degeneration methods after the operated animals had reached maturity. The distribution of S synapses, en passant MH afferents to the central IPN, is normally 95% ipsilateral to their MH of origin in spite of the fact that their axons cross through the contralateral half of the IPN one or more times. The lesions result in a symmetrical distribution of S synapses from the remaining MH. The density of this projection on each side is equal to the normal ipsilateral density of termination. Crest synapses, present in intermediolateral IPN bilaterally, consist of two endings which contact a narrow dendritic process. Normally, the two endings arise one from each MH at 90% of crest synapses, and two from the same MH at 10%. After unilateral MH lesions in neonates, approximately 96% of crest synapses are formed by two axons from the one remaining MH. At only 4% of crest synapses one or both processes is heterologous, that is, of non-MH origin. These findings demonstrate that synapse formation on IPN neurons preferentially favors MH afferents, both normally and when left- right interaction is precluded by a neonatal unilateral lesion. Left- right interactions normally occur at both the level of the left and right sides of the IPN with regard to S synapses and individual left and right habenular afferents at crest synapses. Plasticity at crest synapses is considerably greater in neonates compared to adult rats. Control of these phenomena can be understood as the interaction of multiple factors. These may include specific determinants localized to the presynaptic axons, particularly prior to synaptogenesis and competition for synaptic space, especially with regard to S synapses and perhaps involving synapse elimination. There is also evidence for postsynaptic determinants both in the separation of synaptic types into separate subnuclei and in the formation of crest synapses in the IPN regardless of the presence of normal or reduced numbers of MH afferents, or their total absence.

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