Patients with tachykinin receptor 3 (TACR3) mutations experience pubertal failure, depression, and anxiety, but the underlying mechanisms are not fully understood. In this study, we found that rats with severe anxiety have reduced expression of TACR3 in the hippocampus. We also observed that TACR3 expression in the hippocampus increases in males during sexual development, parallel to changes in anxiety and serum testosterone levels. Although TACR3 is not highly expressed at synapses, its regulation significantly impacts synapse number, function, and plasticity. In particular, inhibiting TACR3 leads to overstimulation of the PKC pathway CaMKII activation, and increased spine density, resulting in strong synaptic connectivity. In anxious rats, TACR3 deficiency is associated with increased spine density in the dentate gyrus and impaired LTP in the same area. We propose that the testosterone-TACR3-PKC pathway mediates the LTP deficits observed in anxious rats.