The collective dynamics of the nascent polypeptide exit tunnel are investigated with the computationally efficient elastic network model using normal mode analysis. The calculated normal modes are considered individually and in linear combinations with different coefficients mimicking the phase angles between modes, in order to follow the mechanistic motions of tunnel wall residues. The low frequency fluctuations indicate three distinct regions along the tunnel-the entrance, the neck, and the exit-each having distinctly different domain motions. Generally, the lining of the entrance region moves in the exit direction, with the exit region having significantly larger motions, but in a perpendicular direction, whereas the confined neck region has rotational motions. Especially the universally conserved extensions of ribosomal proteins L4 and L22 located at the narrowest and mechanistically strategic region of tunnel undergo generally anti- or non-correlated motions, which may have an important role in nascent polypeptide gating mechanism. These motions appear to be sufficiently robust so as to be unaffected by the presence of a peptide chain in the tunnel.