Polyprolines offer many opportunities to study factors influencing peptide and protein folding and structure. Longer chains can adopt two well-defined forms (PPI and PPII), but shorter peptides are quite flexible. To understand in detail the dependence of the secondary structure on the length and the interplay between the side chain and main chain conformation, zwitterionic (Pro)(N) models (with N = 2, 3, 4, 6, 9, 12 and longer inhomogeneous chains) were studied by a combination of the Raman and Raman optical activity (ROA) spectroscopy with the density functional theory (DFT). Potential surfaces were systematically explored for the shorter oligoprolines, and Boltzmann conformational ratios were obtained both for the main chain and the proline ring puckering. The predictions were verified by comparison of the experimental and simulated ROA spectra. The conformer ratios extracted from a decomposition of the experimental ROA into scaled computed spectra well reproduced Boltzmann populations calculated from relative energies. For example, an "A" puckering of the proline ring was found prevalent, relatively independent of the length, whereas the cis-amide backbone form adopted by shorter peptides rapidly disappeared for N > 4. The results are consistent with previous NMR and vibrational circular dichroism (VCD) data. Delocalized exciton vibrations along the peptide chain often enhance the ROA signal, and can thus be used to indicate a longer regular peptide structure. The ROA technique appeared to be very sensitive to the ring puckering; less distinct spectral features were produced by changes in the main chain geometry.