Behavior failures due to previously uncharacterized stimulus-induced modulation appear as neuronal noise

Animals may fail to respond to reliable sensory stimuli because of noise in the neural circuits or modulation by internal states. In locusts, looming-evoked jump escape response (JER) fails in [~]40% of trials, and this failure correlates with multiplexed features of the descending contralateral movement detectors (DCMD) response. Using Hieroglyphus banian, we show that these failures arise from a competing behavioral state, grooming. A light-to-dark transition (LDT) in the JER assay induced prolonged grooming and suppressed JER. Reducing the amplitude of this transition decreased grooming and rescued JER. Electro-mechanical induction of grooming was sufficient to cause JER failure. The grooming state induced by either LDT or electro-mechanical stimulation reduced looming-evoked DCMD responses through divisive gain modulation. Grooming was rare under natural field conditions. Thus, behavioral failures can arise from internal state modulation driven by unobserved stimulus history, rather than stochastic noise in the nervous system. HighlightsO_LIAn unobserved prior sensory event drives failure of escape responses. C_LIO_LILight-to-Dark Transition (LDT) induces a long-lasting grooming state in grasshoppers. C_LIO_LIGrooming state causes divisive gain reduction in the DCMD neuron and escape failures. C_LIO_LIFailures of survival-critical behaviors may reflect state rather than neuronal noise. C_LI Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=68 SRC="FIGDIR/small/739074v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@1f8733eorg.highwire.dtl.DTLVardef@561eb8org.highwire.dtl.DTLVardef@1fae92forg.highwire.dtl.DTLVardef@1e32231_HPS_FORMAT_FIGEXP M_FIG C_FIG Unobserved prior events, rather than neuronal noise, can cause JER failure. Locusts and H. banian fail to evoke JER in response to the looming stimulus in [~]40% of the trials. We show that these failures, correlated to grooming, were caused by the LDT and were rescued when lit. Grooming was sufficient for JER failure, and it was mediated by shunting-inhibition-like modulation of the DCMD response.