Object approach computation by a giant neuron and its relation with the speed of escape in the crab Neohelice

Abstract

Upon detection of an approaching object, the crab Neohelice granulata continuously regulates the direction and speed of escape according to ongoing visual information. These visuomotor transformations are thought to be largely accounted for by a small number of motion-sensitive giant neurons projecting from the lobula (third optic neuropil) towards the supraesophageal ganglion. One of these elements, the monostratified lobula giant neuron of type 2 (MLG2), proved to be highly sensitive to looming stimuli (a 2D representation of an object approach). By performing in vivo intracellular recordings, we assessed the response of the MLG2 neuron to a variety of looming stimuli representing objects of different sizes and velocities of approach. This allowed us to: (1) identify some of the physiological mechanisms involved in the regulation of the MLG2 activity and test a simplified biophysical model of its response to looming stimuli; (2) identify the stimulus optical parameters encoded by the MLG2 and formulate a phenomenological model able to predict the temporal course of the neural firing responses to all looming stimuli; and (3) incorporate the MLG2-encoded information of the stimulus (in terms of firing rate) into a mathematical model able to fit the speed of the escape run of the animal. The agreement between the model predictions and the actual escape speed measured on a treadmill for all tested stimuli strengthens our interpretation of the computations performed by the MLG2 and of the involvement of this neuron in the regulation of the animal's speed of run while escaping from objects approaching with constant speed.

The predator and prey behaviors of crabs: from ecology to neural adaptations

“…In contrast, the apparently unique MLG2 neuron, with its receptive field that encompasses the whole 360 deg, was found to respond to stimuli approaching from anywhere around the crab, and to encode looming information for images expanding beyond 35 deg. Using a wide variety of stimulus dynamics, we found that the MLG2 neuron faithfully encodes the angular velocity of looming stimuli, and thus conveys the information that is used by the animal to continuously adjust its running speed (Oliva and Tomsic, 2016).…”

Multielectrode Recordings From Identified Neurons Involved in Visually Elicited Escape Behavior

“…However, the response of these two cells to looming stimuli was very different. On one hand, the MLG2 neuron increases the firing rate according to the dynamic of image expansion (Oliva et al, 2007 ; Oliva and Tomsic, 2016 ). This is illustrated in the intracellularly recorded trace of Figure 3B .…”

“…The cell morphologies shown in panels ( A,F ) are from Medan et al ( 2007 ). Data shown in panels ( B,D ) have been modified from Oliva and Tomsic ( 2016 ). Data in panels ( G,I ) have been modified from Oliva ( 2010 ).…”

“…Contrasting, MLG2 is likely a unique element, with a receptive field covering the entire visual space (Medan et al, 2007 ). This neuron has been shown to play a central role in regulating the animal’s speed of run according to the visual dynamic of approaching stimuli (Oliva and Tomsic, 2016 ). The BLG1 class is composed of a discrete number of elements (Medan et al, 2007 ; Scarano et al, 2018 ), which might participate in encoding information regarding stimulus elevation (Tomsic, 2016 ).…”

Neuronal ON/OFF Motion Detection Circuits Underlying Looming-Evoked Escape Behavior inDrosophila

“…Escape behaviors to looming stimuli have been particularly well investigated in two other family of arthropods: grasshoppers and crabs. In contrast to Drosophila, the visual inputs to looming detection neurons in these animals are not thought to be directionally selective Gabbiani 2010, 2012;Medan et al 2007;Oliva and Tomsic 2016). Yet, the computations carried out in Drosophila, grasshoppers, and crabs appear very similar at the behavioral level Oliva and Tomsic 2012;von Reyn et al 2014).…”