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.

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

“…Fig. 6 shows the average firing rate as a function of the angular size θ(t-δ n ), angular velocity θ′(t-δ n ) and angular acceleration θ″(t-δ n ), assuming a neural response delay of δ n =35 ms at 22-24°C according to Medan et al (2007) (same temperature as in the present study) and to our delay measurements for angular velocities greater than 5 deg s −1 (Fig. 4A).…”

“…Responses of the MLG2 neuron to looming stimuli from different directions Medan et al (2007) performed the first morphological and physiological characterization of the MLG2 neuron. Fig.…”

Predation risk modifies behaviour by shaping the response of identified brain neurons

“…Wide-field tangential neurons of the lobula can be identified based on their stronger response to motion stimuli compared with stationary changes of illumination (Berón de Astrada and Tomsic, 2002;Medan et al, 2007). Once the identity of a LG neuron was established, a black curtain was lowered to prevent uncontrolled visual stimulation and the animal was left undisturbed for 10 min before the experiment began.…”

“…An extensive amount of evidence indicates that the crab response to VDS involves a group of at least four distinct classes of motion-sensitive lobula giant (LG) neurons. These are central elements that arise in the lobula (third optic neuropile) and project their axon through the protocerebral tract, presumably to premotor centres in the midbrain (Berón de Astrada and Tomsic, 2002;Medan et al, 2007Medan et al, , 2015Sztarker et al, 2005). The response strength of LG neurons correlates closely with the intensity of the escape response of crabs to VDS across a broad range of conditions Tomsic, 2008, 2011;Tomsic et al, 2003).…”

“…The time course of LG responses also correlates well with the temporal dynamics of the escape response (Berón de Astrada et al, 2013;Oliva and Tomsic, 2014;Tomsic et al, 2009), suggesting that these neurons process most of the relevant visual information that drives the escape behaviour. Three classes of LG neurons respond not only to visual information but also to proprioceptive input from the legs (Berón de Astrada and Tomsic, 2002;Medan et al, 2007). This may allow them to process some of the contextual information during predator escape, such as path integration information, which has been shown to influence the escape and burrow defence behaviour of fiddler crabs in the field (Hemmi and Zeil, 2003a,b).…”