Computation of object approach by a system of visual motion-sensitive neurons in the crabNeohelice

Abstract

Similar to most visual animals, crabs perform proper avoidance responses to objects directly approaching them. The monostratified lobula giant neurons of type 1 (MLG1) of crabs constitute an ensemble of 14-16 bilateral pairs of motion-detecting neurons projecting from the lobula (third optic neuropile) to the midbrain, with receptive fields that are distributed over the extensive visual field of the animal's eye. Considering the crab Neohelice (previously Chasmagnathus) granulata, here we describe the response of these neurons to looming stimuli that simulate objects approaching the animal on a collision course. We found that the peak firing time of MLG1 acts as an angular threshold detector signaling, with a delay of δ = 35 ms, the time at which an object reaches a fixed angular threshold of 49°. Using in vivo intracellular recordings, we detected the existence of excitatory and inhibitory synaptic currents that shape the neural response. Other functional features identified in the MLG1 neurons were phasic responses at the beginning of the approach, a relation between the stimulus angular velocity and the excitation delay, and a mapping between membrane potential and firing frequency. Using this information, we propose a biophysical model of the mechanisms that regulate the encoding of looming stimuli. Furthermore, we found that the parameter encoded by the MLG1 firing frequency during the approach is the stimulus angular velocity. The proposed model fits the experimental results and predicts the neural response to a qualitatively different stimulus. Based on these and previous results, we propose that the MLG1 neuron system acts as a directional coding system for collision avoidance.

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

“…In this section we study some physiological phenomena previously observed in the locust's LGMD neuron Gabbiani, 2010, 2012) and in MLG1 neurons of the crab (Oliva and Tomsic, 2014), which proved to be relevant to the codification of looming stimuli.…”

“…Following experiences from our previous studies (e.g. Oliva et al, 2007;Oliva and Tomsic, 2014), we began stimulation after the animal had remained visually undisturbed for 3 min inside the setup. In all trials, the stimulus remained stationary for 30 s at its initial position before starting to increase in size.…”

“…Such neurons are commonly referred as looming sensitive neurons (LSNs). LSNs have been found in pigeons (Wang and Frost, 1992), fish (Preuss et al, 2006), monkeys (Maier et al, 2004) and different arthropod species such as locusts (Rind and Simmons, 1992;Gabbiani et al, 1999;Gray et al, 2010), flies (Borst, 1991;Fotowat et al, 2009), crayfish (Glantz, 1974) and crabs Oliva and Tomsic, 2014). But, how is the visual information of an approaching object actually processed, encoded and conveyed by LSNs to contribute to avoidance behaviors?…”

“…In conjunction, the ensemble of MLG1s covers the 360 deg visual field seen by each eye of the crab Sztarker et al, 2005). MLG1s have been recently characterized in terms of their responses to looming stimuli and their possible role in the control of the direction and speed of escape (Medan et al, 2015), and their responses have been modeled (Oliva and Tomsic, 2014). Therefore, within this work we focused on the other cell type, the monostratified lobula giant of type 2 (MLG2), which is a much larger neuron than the MLG1s.…”

“…There is apparently only one MLG2 per lobula Sztarker et al, 2005). In order to compare the performance of the MLG2 neuron with the previously investigated performance of MLG1 neurons of the crab, in this study we applied the same methodology that we employed in our previous study on the MLG1 neurons (Oliva and Tomsic, 2014).…”