A new multidimensional thermodynamic integration method is applied to investigate free energy surfaces of alanine (Ala) and alpha-methylalanine (Aib) homopeptides in the helical region. In this approach a single molecular dynamics simulation with all phi and psi dihedrals kept fixed yields the free energy gradient with respect to all the fixed conformational coordinates. For regular structures of model peptides (Ala)(n), and (Aib)(n), where n = 6, 8, 10 and Aib is alpha-methylalanine in vacuum, free energy maps in phi-psi space are calculated and used to roughly locate free energy minima. For (Ala)(n), alpha-helical minima are found for n = 6, 8, 10 and a pi-helical minimum exists for n = 10, while all studied (Aib)(n), peptides have stable alpha- and 3(10)-helical states. The locations of the free energy minima are further refined by the novel procedure of free energy optimization by steepest descent down the gradient, leading to structures in excellent agreement with experimental data. The stability of the minima with respect to deformations is studied by analysis of second derivatives of the free energy surface. Analysis of free energy components and molecular structures uncovers the molecular mechanism for the propensity of Aib peptides for the 3(10)-helix structure in the interplay between the quality and quantity of hydrogen bonds. The (Ala)(10) alpha-helix is favored over the 3(10)-helix by all energy terms, exhibiting lower internal strain, lower van der Waals repulsion, and more favorable electrostatic interactions. Although the 3(10)-helix has one more hydrogen bond, in (Ala)(n) each individual helical hydrogen bond is weaker in the 3(10)-helix than in the alpha-helix. In (Aib)(n) peptides the added bulk of the a-methyls subtly deforms the helices, inducing larger internal strain and larger van der Waals repulsion than in corresponding (Ala)(n), structures and making the (Aib)(n) hydrogen bond geometry better in the 3(10)- than in the alpha-helix. The synergistic effect of greater number of hydrogen bonds and improved interactions within each bond strongly stabilizes the (Aib)(n) 3(10)-helix, making it the favored structure for short peptides.