Neurons in the chicken nucleus laminaris (NL), the third-order auditory neurons that detect the interaural time differences that enable animals to localize sounds in the horizontal plane, receive glutamatergic excitation from the cochlear nucleus magnocellularis (NM) and GABAergic inhibition from the ipsilateral superior olivary nucleus. Here, we investigate metabotropic glutamate receptor (mGluR)- and -aminobutyric acid B receptor (GABA_BR)-mediated modulation of synaptic transmission in NL neurons. Gramicidin-perforated recordings from acute brainstem slice preparations revealed that the reversal potential of the GABAergic responses in NL neurons was more depolarized than the spike threshold. Activation of the GABAergic input produced a mix of inhibitory and excitatory actions in NL neurons. The inhibitory action is known to be critical in improving the acuity of temporal processing of sounds. The excitatory action, however, would reduce the phase locking fidelity of NL neurons in response to their excitatory inputs from the NM. We demonstrate that activation of presynaptic mGluRs or GABA_BRs by either exogenous agonists or synaptically released neurotransmitters reduced the GABAergic responses, preventing the excitatory action of GABA while leaving the inhibitory action intact. Unlike most CNS synapses, the glutamatergic transmission in the NL was not modulated by either mGluRs or GABA_BRs, indicating that fixed (non-modulatory) excitatory inputs to the NL may be optimal for coincidence detection. This study contributes to our understanding of how selective neuromodulation is achieved to suit a particular function of neuronal circuits in the brain.