Direction Selective Neurons Responsive to Horizontal Motion in a Crab Reflect an Adaptation to Prevailing Movements in Flat Environments

Abstract

All animals need information about the direction of motion to be able to track the trajectory of a target (prey, predator, cospecific) or to control the course of navigation. This information is provided by direction selective (DS) neurons, which respond to images moving in a unique direction. DS neurons have been described in numerous species including many arthropods. In these animals, the majority of the studies have focused on DS neurons dedicated to processing the optic flow generated during navigation. In contrast, only a few studies were performed on DS neurons related to object motion processing. The crab Neohelice is an established experimental model for the study of neurons involved in visually-guided behaviors. Here, we describe in male crabs of this species a new group of DS neurons that are highly directionally selective to moving objects. The neurons were physiologically and morphologically characterized by intracellular recording and staining in the optic lobe of intact animals. Because of their arborization in the lobula complex, we called these cells lobula complex directional cells (LCDCs). LCDCs also arborize in a previously undescribed small neuropil of the lateral protocerebrum. LCDCs are responsive only to horizontal motion. This nicely fits in the behavioral adaptations of a crab inhabiting a flat, densely crowded environment, where most object motions are generated by neighboring crabs moving along the horizontal plane.

Dragonfly visual neurons selectively attend to features in naturalistic scenes

“…recorded from the animal's left optic lobe,Figure 2A, upper trace) and excitation for leftwardmoving targets(Figure 2A, lower trace). Similar direction opponency has been previously observed in dragonfly STMDs (O'Carroll 1993) and more recently described in crab LCDC neurons, which exhibit some functional similarity to the dragonfly STMDs(Scarano et al 2020). Like CSTMD1, BSTMD2 prefers small targets (Figure 2B, top) over elongated features (Figure 2B, bottom) but still shows modest responses.As previously described(Bolzon et al, 2009) CSTMD1 also responds to targets in both visual hemifields, but in this case with a clear distinction between excitatory and inhibitory responses at the central midline.…”

Multielectrode Recordings From Identified Neurons Involved in Visually Elicited Escape Behavior

“…Note the differences in the scale times among panels. Data in panel (A) have been modified from Scarano et al ( 2020 ). See the text for further details.…”

“…Recently, we have described a novel group of large neurons of the crab that exhibit a remarkable directional preference for visual stimuli moving along the horizontal plane. Because of their arborizations in the lobula and the lobula plate, we called these cells lobula complex directional cells (LCDC; Scarano et al, 2020 ). The LCDC response to a moving square is characterized by a clear increase of spike discharge in one direction, the so-called preferred direction, and a hyperpolarization with suppression of spontaneous spikes in the opposite direction called the null direction.…”

“…Yet, extracellular multichannel recordings in arthropods have mostly been made from unidentified cells, and attempts to recognize specific neurons based on matching the responses to particular stimuli with those previously obtained from intracellular recordings have largely failed (e.g., Bhavsar et al, 2015). By recording with the duo-tetrode from the lobula we were able to confidently identify two of the four types of LG neurons that have been described so far (e.g., Medan et al, 2007), as well as the recently described directional giant neurons (Scarano et al, 2020). Among the four classes of LG neurons, the MLG2 and BLG2 recognized in the present study are the largest lobula neurons, whose arborizations profusely extend all over the neuropil (Medan et al, 2007).…”

“…This study represents our first approach to using multielectrode recording in the crab. For this reason, we included in our experiments stimuli that proved to be effective both for identifying different lobula neurons (Medan et al, 2015 ; Tomsic et al, 2017 ; Scarano et al, 2018 , 2020 ) and for eliciting a variety of behavioral responses in this animal, such as escape response (Oliva and Tomsic, 2012 ; Scarano and Tomsic, 2014 ), predatory response (Gancedo et al, 2020 ) and optomotor response (Barnatan et al, 2019 ). Computer-generated visual stimuli were projected on a computer screen (Samsung S20C300L) placed at a distance of 20 cm, covering the frontolateral right side of the animal.…”