This study extended motor imagery theories by establishing specificity and verification of expected brain activation patterns during imagery. Eighteen female participants screened with the Movement Imagery Questionnaire-3 (MIQ-3) as having good imagery abilities were scanned to determine the neural networks active during an arm rotation task. Four experimental conditions (i.e., KINESTHETIC, INTERNAL Perspective, EXTERNAL Perspective, and REST) were randomly presented (counterbalanced for condition) during three brain scans. Behaviorally, moderate interscale correlations were found between the MIQ-3 and Vividness of Movement Imagery Questionnaire-2, indicating relatedness between the questionnaires. Partially confirming our hypotheses, common and distinct brain activity provides initial biological validation for imagery abilities delineated in the MIQ-3: kinesthetic imagery activated motor-related areas, internal visual imagery activated inferior parietal lobule, and external visual imagery activated temporal, but no occipital areas. Lastly, inconsistent neuroanatomical intraindividual differences per condition were found. These findings relative to recent biological evidence of imagery abilities are highlighted.