Failure to establish B-cell tolerance to self-antigens leads to the development of antibody-mediated autoimmunity. Early work in B-cell receptor transgenic systems indicated that self-reactive B cells which escape negative selection are rendered anergic by peripheral tolerance. Although these models provided valuable insights, the mechanisms underlying peripheral B-cell tolerance for a normal polyclonal repertoire with a range of antigen affinities remain poorly understood due to a lack of tools to study polyclonal B-cell responses in vivo. To test the extent of tolerance in a polyclonal repertoire, mice expressing membrane-bound ovalbumin (OVA) ubiquitously as a model self-antigen (actin.mOVA) or wild-type controls were immunized with OVA and various adjuvants. Surprisingly, OVA-specific IgG1, albeit of lower affinity and reduced titre relative to wild-type controls, could be detected in immunized actin.mOVA mice, in a graded manner that reflected the strength of adjuvant used. Because antigen-specific B cells are present in a polyclonal repertoire at only very low frequency, we developed a novel B-cell tetramer approach to detect OVA-specific B cells. In line with OVA-specific antibody levels, expansion of OVA-specific B cells in actin.mOVA mice was also reduced relative to wild-type littermates. OVA-specific ELISpots also revealed fewer specific antibody-forming cells in actin.mOVA mice. These findings indicate the capacity of peripheral tolerance to limit responses to self-antigens, but suggest B cell tolerance is incomplete and can be partially broken, particularly with strong adjuvants. Because immunological memory is a byproduct of responsiveness, and involved in autoimmunity, we wondered whether actin.mOVA mice formed OVA-specific B cell memory. Although actin.mOVA mice harbour switched-memory OVA-specific B cells following immunization, secondary responses during re-challenge may be impaired, implying that formation of self-reactive B cell memory is silenced by peripheral tolerance following initial activation. The tools and observations from these studies are important for characterising antigen-specific B cell tolerance.