Journal Article

Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs

Williamson, W Ryan, Nern, Aljoscha, Wu, Ming, Morimoto, Mai M, Reiser, Michael B, Rubin, Gerald M, Card, Gwyneth M

2016

Overview

Visual projection neurons (VPNs) provide an anatomical connection between early visual processing and higher brain regions. Here we characterize lobula columnar (LC) cells, a class of Drosophila VPNs that project to distinct central brain structures called optic glomeruli. We anatomically describe 22 different LC types and show that, for several types, optogenetic activation in freely moving flies evokes specific behaviors. The activation phenotypes of two LC types closely resemble natural avoidance behaviors triggered by a visual loom. In vivo two-photon calcium imaging reveals that these LC types respond to looming stimuli, while another type does not, but instead responds to the motion of a small object. Activation of LC neurons on only one side of the brain can result in attractive or aversive turning behaviors depending on the cell type. Our results indicate that LC neurons convey information on the presence and location of visual features relevant for specific behaviors. Many animals rely heavily on what they can see to interact with the world around them. But how does the brain use such visual information to guide behavior? Light-sensitive neurons in the eye cannot distinguish between the visual signals associated with, say, an approaching predator or a source of food. Yet the brain can make this distinction. Networks of neurons in the brain perform computations to extract information from a visual scene that indicates the need for a particular behavior, such as an escape response. These networks are found in regions of the brain that communicate closely with the eyes. Cells known as visual projection neurons then relay the output of these networks to more central parts of the brain. By studying visual projection neurons, it is possible to work out what the eye tells the brain, and how the brain uses this information to control behavior. The fruit fly Drosophila is a suitable model organism in which to study these phenomena. This insect shows a range of behavioral responses to visual stimuli, and can be studied using sophisticated genetic tools. Wu, Nern et al. set out to explore how a group of visual projection neurons known as lobula columnar cells help fruit flies respond appropriately to visual stimuli. Experiments revealed that individual subtypes of lobula columnar cells convey information about the presence and general location of specific visual features. Wu, Nern et al. identified a number of lobular columnar subtypes involved in triggering escape responses to specific stimuli – such as walking backwards or taking off in flight – as well as others that can trigger the flies to approach a target. A next step is to map the circuits of neurons that act upstream and downstream of lobula columnar cells. This can help to reveal how these neurons detect specific visual features and how the fly then chooses and executes an appropriate behavior in response. Such studies in flies can provide insights into general principles of how brains use sensory information to guide behavior.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Avoidance behavior / Behavior / Behavior, Animal / Brain / Calcium imaging / Drosophila / Drosophila - anatomy & histology / Drosophila - physiology / feature detection / Information processing / Insects / lobula / loom detection and avoidance behaviors / Neural circuitry / Neuroimaging / Neurons / Neurons - cytology / Neurons - physiology / Neuroscience / optic glomeruli / Optical Imaging / Optogenetics / Physiological aspects / retinotopy / Software / visual behavior / Visual cortex / Visual Pathways - anatomy & histology / Visual Pathways - physiology / Voltage-Sensitive Dye Imaging