Using electrophysiology combined with immunohistochemistry, we find that endogenously released opioids directly activate a potassium conductance in Im neurons via MOR. We also find that whilst exogenous Met-enkephalin (ME) and selective MOR, and DOR agonists reduced glutamate release from BLA synaptic inputs, endogenously released opioids only inhibit glutamate release through DOR. These endogenous opioid actions could be potentiated by reducing endogenous opioid breakdown by peptidases or by a positive allosteric modulator (PAM) specific for DOR. These findings indicate that endogenously released opioids tightly regulate the excitability and synaptic activation of Im neurons through two different receptors. Further, this regulation is not limited to high intensity synaptic activity, suggesting a role for endogenously released opioids as regulators of moment-to-moment signalling within a dynamic neuronal network. This would be expected to contribute to the role of endogenous opioids in fear learning and anxiety.