Pauses during communication release behavioral habituation through recovery from synaptic depression

Abstract

During interactive communication, animals occasionally cease producing communication signals. The behavioral significance of resumed communication signals following a cessation, or silent pause, has been described in human speech: word recognition by listeners is enhanced after silent pauses, and speakers tend to place such pauses prior to words that are contextually unpredictable and that therefore have high information content.1-5 How central nervous systems process signals following pauses differently from signals during continuous communication has not been studied at a cellular level. Here we studied behavioral and neurophysiological impacts of pauses during electric communication in mormyrid fish. We found that isolated fish produced fewer and shorter pauses than fish housed in pairs, and that fish tended to produce burst displays immediately following pauses. In the electrosensory pathway, sensitivity to pauses first arose in the midbrain posterior exterolateral nucleus (ELp): evoked field potentials were enhanced as pause duration increased, with a time constant of ∼1 s. Intracellular recording from single ELp neurons suggested that this increased sensitivity resulted from a pause-associated recovery from synaptic depression that was induced by the preceding stimulation. Behavioral responses were also facilitated by longer pauses, with a similar time constant of ∼1 s. Further, during natural electric communication between pairs of fish, the insertion of artificial pauses resulted in increased signaling by the receiving fish immediately following the pause. Thus, our results suggest that pauses during communication release sensory circuits from synaptic depression, thereby maximizing the physiological and behavioral effects of subsequent communication signals.