Small Insect Nervous Systems Process Multi-Dimensional Sensory Data During Target Location

A pregnant female Ormia ochracea fly has a challenging problem to solve. She must listen for the song of male crickets, locate one in the dark, and use him as a host for her developing offspring.

But first, she has to decide whether that song is worth chasing.

New research published in the Journal of Experimental Biology reveals that the answer is more complicated than scientists previously understood. Researchers from St. Olaf College found that female Ormia ochracea - small, yellow, crepuscular flies who implant crickets with their larvae - do not simply recognize attractive cricket songs based on their beat, or pulse rate. Instead, these flies evaluate multiple aspects of the songs' temporal features. In fact, two songs with the same pulse rate can result in dramatically different responses.

"Two songs can have exactly the same pulse rate but mean very different things to the fly," said lead author Lauren Bitner, a postbaccalaureate research associate in the Lee Lab of Neural Systems and Behavior at St. Olaf College. "What matters isn't just how quickly the sound pulses repeat, but how the fly pays attention to the way the rhythm is constructed."

The research found that:

• Female flies were most attracted to cricket songs with a particular combination of sound pulses and pauses.

• The flies did not recognize attractive songs based on song pulse rate alone, but instead listened to multiple features of the song's rhythm.

Building Cricket Songs One Pulse at a Time

Cricket songs may sound simple, but their rhythms can be composed in many ways. Each song consists of sound pulses separated by periods of silence. A particular pulse rate can therefore be produced by short pulses and longer silences, or longer pulses and shorter silences.

The researchers took advantage of this distinction by creating artificial cricket songs where they were able to independently vary the duration of sound pulses, and the silence between pulses. They then presented these songs to pregnant female Ormia ochracea and measured how strongly the flies respond to these songs.

The experiments revealed a striking pattern. Pulse rate predicted some of the flies' behavior but it could not fully explain which songs they preferred. Songs with the same pulse rate sometimes elicited very different responses depending on the specific combination of sound and silence.

Instead of listening for a single "magic number" of pulses per second, the flies appear to recognize relevant cricket songs based on combinations of temporal features.

A Tiny Brain Solving a Complex Recognition Problem

For Ormia ochracea, finding crickets in nature is a real challenge. The flies have evolved a sensitive auditory system to eavesdrop on cricket communication signals to find a suitable host for the development of their larval young, but not every sound leads to an appropriate host cricket. Correctly identifying the right song, therefore, can have direct consequences for reproduction. The results suggest that flies can solve this recognition problem by considering several features of a signal at once. Even their small, relatively simple nervous system can process this information in a combined way.

It's tempting to imagine that a tiny fly with a tiny nervous system must use a very simple rule. What we're finding is that these flies may be integrating multiple pieces of information when deciding which sounds to pursue."

Norman Lee, Study Senior Author and Associate Professor of Biology and Director of the Neuroscience Program, St. Olaf College

The discovery opens many interesting questions, including: where in the fly's nervous system does this song selectivity or recognition arise? Ormia ochracea are also found in several places in the continental U.S. and in Hawaii. In each of these populations, these flies may parasitize different host cricket species that produce calling songs with drastically different temporal structure. What temporal features might these other populations of Ormia ochracea be assessing to recognize their hosts?

Ultimately, the research addresses a much broader problem than how a fly recognizes a cricket. The research team suggests future exploration of how animals constantly need to decide which sights, sounds, and smells matter. Those signals are rarely defined by a single feature. Understanding how Ormia ochracea combines information across a cricket song provides a window into a fundamental problem faced by nervous systems of all sizes: how the brain turns complex sensory information into a decision about what to do next.

This research was supported by a National Science Foundation CAREER grant. The Lee Lab at St. Olaf studies how animals sense, process, and respond to the world around them; specifically through acoustic communication. Lee leads an undergraduate research team and collaborates with other biologists across the United States and Canada.