Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Abstract

Modulation of sensitivity to sensory cues by experience is essential for animals to adapt to a changing environment. Sensitization and adaptation to signals of the same modality as a function of experience have been shown in many cases, and some of the neurobiological mechanisms underlying these processes have been described. However, the influence of sensory signals on the sensitivity of a different modality is largely unknown. In males of the noctuid moth, Spodoptera littoralis, the sensitivity to the femaleproduced sex pheromone increases 24 h after a brief preexposure with pheromone at the behavioral and central nervous level. Here we show that this effect is not confined to the same sensory modality: the sensitivity of olfactory neurons can also be modulated by exposure to a different sensory stimulus, i.e., a pulsed stimulus mimicking echolocating sounds from attacking insectivorous bats. We tested responses of preexposed male moths in a walking bioassay and recorded from neurons in the primary olfactory center, the antennal lobe. We show that brief exposure to a bat call, but not to a behaviorally irrelevant tone, increases the behavioral sensitivity of male moths to sex pheromone 24 h later in the same way as exposure to the sex pheromone itself. The observed behavioral modification is accompanied by an increase in the sensitivity of olfactory neurons in the antennal lobe. Our data provide thus evidence for cross-modal experience-dependent plasticity not only on the behavioral level, but also on the central nervous level, in an insect.bat sound | plant odor | sexual behavior | intracellular recording A nimals live in an ever-changing environment and must be able to adapt their behavior in response to highly varying sensory cues. One way to achieve such adaptive behavior is through plasticity of the nervous system, whereby modifications can be induced depending on sensory input. Previous studies have shown that exposure to environmental signals during development and in early adult life might influence the precise design and sensitivity of the targeted sensory system (1-3). The development of the peripheral and central visual, auditory, somatosensory, and olfactory systems in vertebrates has been shown to be highly influenced by experience (e.g., refs. 4-11) and regulated by neurogenesis and network remodeling with, for example, axon growth, the increase of the number of synaptic connections, and the strengthening of existing synapses (ref. 1 and references therein; ref. 12).Different strategies to achieve high sensitivity for abundant and/ or important signals have evolved. One way is limited attention, whereby an animal focuses on a specific sensory system, or even on a specific type of sensory signal, whereas other, simultaneously occurring information signals might be less attended (13,14). Experience of sensory input with a behaviorally important stimulus could also elicit long-term changes, which improve the insect's ability to respond to that specific stimulus (e.g., ref. 15). Furthermore, brief s...

Brief Exposure to Sensory Cues Elicits Stimulus-Nonspecific General Sensitization in an Insect

“…Interestingly, although the sensitivity of AL neurons to pheromone was recently shown to change after pheromone and bat sound pre-exposure [19], [33], our new data allow us to exclude early processing stages (the antennal and AL level) to be at the origin of gustatory-evoked pheromone sensitization.…”

Neurobiology of acoustically mediated predator detection

“…Consistent with this, an identified sound-sensitive brain neuron also has extensive processes in this area (Pfuhl et al 2014). Another brain neuron that responds to acoustic stimuli has extensive axonal processes in the antennal lobe (Zhao et al 2013), and might play a role in mediating neural and behavioral interactions between acoustic and olfactory stimuli (Skals et al 2005;Anton et al 2011). …”

Simple ears – flexible behavior: Information processing in the moth auditory pathway

“…Accordingly, Skals et al (2005) showed that the escape response is delayed when simultaneously perceiving pheromones. Recently, a possible mechanism through which auditory stimuli can modulate the olfactory perception was sug-gested (Anton et al, 2011;Zhao et al, 2013).…”

“…This ipsilateral neuron type, which was morphologically and physiologically identified in two geographically isolated species of heliothine moths, innervates all antennal-lobe glomeruli and extends numerous fine processes in the dorso-medial protocerebrum. Also of interest, Anton et al (2011) found, in Spodoptera littoralis, that antennallobe projection neurons were sensitized one day after the moths had been exposed to bat sounds. Projection neurons of moths being exposed to control sounds, however, showed no sensitization.…”