In this study, we address the impact of temperature acclimation on neuronal properties in the Mauthner (M-) system, a brainstem network that initiates the startle-escape behavior in goldfish. The M-cell can be studied at cellular and behavioral levels since it is uniquely identifiable physiologically within the intact vertebrate brain, and a single action potential in this neuron determines whether a startle response will occur, as well as the direction of the escape. Using animals acclimated to 15°C as a control, 25°C-acclimated fish showed a significant increase in escape probability and a decrease in the ability to discriminate escape directionality. Intracellular recordings demonstrated that M-cells in this population possessed decreased input resistance, and reduced strength and duration of inhibitory inputs. In contrast, fish acclimated to 5°C were behaviorally similar to 15°C fish, and had increased input resistance, increased strength of inhibitory transmission, and reduced excitatory transmission. We show here that alterations in the balance between excitatory and inhibitory synaptic transmission in the M-cell circuit underlie differences in behavioral responsiveness in acclimated populations. Specifically, during warm acclimation, synaptic inputs are weighted on the side of excitation and fish demonstrate hyperexcitability and reduced left-right discrimination during rapid escapes. In contrast, cold acclimation results in transmission weighted on the side of inhibition, and these fish are less excitable and show improved directional discrimination.