Characterization of Lobula Giant Neurons Responsive to Visual Stimuli That Elicit Escape Behaviors in the CrabChasmagnathus

Abstract

In the grapsid crab Chasmagnathus, a visual danger stimulus elicits a strong escape response that diminishes rapidly on stimulus repetition. This behavioral modification can persist for several days as a result of the formation of an associative memory. We have previously shown that a generic group of large motion-sensitive neurons from the lobula of the crab respond to visual stimuli and accurately reflect the escape performance. Additional evidence indicates that these neurons play a key role in visual memory and in the decision to initiate an escape. Although early studies recognized that the group of lobula giant (LG) neurons consisted of different classes of motion-sensitive cells, a distinction between these classes has been lacking. Here, we recorded in vivo the responses of individual LG neurons to a wide range of visual stimuli presented in different segments of the animal's visual field. Physiological characterizations were followed by intracellular dye injections, which permitted comparison of the functional and morphological features of each cell. All LG neurons consisted of large tangential arborizations in the lobula with axons projecting toward the midbrain. Functionally, these cells proved to be more sensitive to single objects than to flow field motion. Despite these commonalities, clear differences in morphology and physiology allowed us to identify four distinct classes of LG neurons. These results will permit analysis of the role of each neuronal type for visually guided behaviors and will allow us to address specific questions on the neuronal plasticity of LGs that underlie the well-recognized memory model of the crab.