In this study, sheep oocyte-cumulus cell complexes derived from medium antral follicles (M-OCC) were in vitro matured alone or in co-culture with complexes derived from small antral follicles (S-OCC) to investigate the contribution of cumulus cells (CC) and oocytes to the process of oocyte meiotic maturation and cumulus expansion (CE). Experiments were conducted with or without gonadotropins (FSH/LH). Regardless of culture conditions, about 12% of S-oocytes reached the metaphase II stage (MII), and S-CC showed a low degree of CE. In contrast, both maturational processes were significantly stimulated by gonadotropins in M-OCC. However, about 48% of S-oocytes progressed to MII and S-CC expanded following co-culture with gonadotropin-stimulated M-OCC and M-CC, but not with mural granulosa cells. Both maturational processes were inhibited when S-OCC were co-cultured with M-denuded oocytes, or when S-denuded oocytes were co-cultured with M-CC. The capacity of these paracrine factor(s) to activate MAPK pathway in somatic and germ cells of S-complexes was investigated. It was found that MEK/MAPK phosphorylation levels in M-OCC but not in S-OCC were significantly increased by gonadotropins, firstly in cumulus cells and later in the oocytes. Kinase phosphorylations were activated only in S-oocytes co-cultured with M-OCC or M-CC. These results demonstrate that soluble factor(s) specifically produced by M-CC are capable to induce meiotic maturation and CE in S-complexes by acting via cumulus cells. These factor(s) can induce MAPK activation only in S-oocytes, whose meiotic arrest could be due to the inability of surrounding cumulus cells to respond to gonadotropin stimulation.