The ultrasound acoustic startle response (ASR) of crickets (Teleogryllus oceanicus) is a defense against echolocating bats. The ASR to a test pulse can be habituated by a train of ultrasound prepulses. We found that this conditioning paradigm modified both the gain and the lateral direction of the startle response. Habituation reduced the slope of the intensity/response relationship but did not alter stimulus threshold, so habituation extended the dynamic range of the ASR to higher stimulus intensities. Prepulses from the side (90 degrees or 270 degrees azimuth) had a priming effect upon the lateral direction of the ASR, increasing the likelihood that test pulses from the front (between -22 degrees and +22 degrees ) would evoke responses towards the same side as prepulse-induced responses. The plasticity revealed by these experiments could alter the efficacy of the ASR as an escape response and might indicate experience-dependent modification of auditory perception. We also examined stimulus control of habituation by prepulse intensity or direction. Only suprathreshold prepulses induced habituation. Prepulses from one side habituated the responses to test pulses from either the ipsilateral or contralateral side, but habituation was strongest for the prepulse-ipsilateral side. We suggest that habituation of the ASR occurs in the brain, after the point in the pathway where the threshold is mediated, and that directional priming results from a second process of plasticity distinct from that underlying habituation. These inferences bring us a step closer to identifying the neural substrates of plasticity in the ASR pathway.