Unraveling the functional organization of lobula complex in the mantis brain by identification of visual interneurons

Abstract

The praying mantis shows broad repertories of visually guided behaviors such as prey recognition and defense against collision. It is likely that neurons in the lobula complex (LOX), the third visual neuropil in the optic lobe, play significant roles in these behaviors. The LOX in the mantis brain consists of five neuropils: outer lobes 1 and 2 (OLO1 and OLO2); anterior lobe (ALO); dorsal lobe (DLO); and stalk lobe (SLO), and ALO comprise ventral and dorsal subunits, ALO‐V and ALO‐D. To understand the functional organization of LOX, intracellular electrodes were used for recording from and staining neurons in these neuropils of the mantis (Tenodera aridifolia). The neurons belonged to three categories based on their response properties and morphologies. First, tangential ALO‐V neurons projecting to ventromedial neuropils (VMNP) (TAproM1 and 2), tangential DLO (or ALO‐D) neurons projecting to VMNP (TDproM1 and 2), and tangential ALO‐V centrifugal neurons (TAcen) all showed directional sensitivity and sustained excitation to gratings drifting in preferred direction (outward–downward, inward–upward, outward–upward, inward–downward, and inward, respectively). Second, tangential OLO neurons projecting to VMNP or ventrolateral neuropils (VLNP) (TOproM or TOproL), columnar OLO commissural neurons (COcom), and SLO commissural neurons (Scom) all showed strong excitation to 2°–8° moving squares but little excitations to drifting gratings. COcom and SLO neurons ramified in both left and right LOX. Last, the class of tangential ALO‐V neurons projecting to VLNP (TAproL1, 2, and 3) responded best to looming circles and showed little excitation to receding, darkening, and lightening circles.

Binocular responsiveness of projection neurons of the praying mantis optic lobe in the frontal visual field

“…We recorded from five different projection neurons with input in the most distal neuropils of the praying mantis lobula complex (LOX): the outer lobe 1 (OLO1) and the outer lobe 2 (OLO2). Two of the cells belonged to the same cell type, TOpro1 (tangential projection neuron of the outer lobes; (Rosner et al 2017)) also called L7-cell by (Berger 1985) or TOproM1 by (Yamawaki 2019) to additionally highlight its output ramifications within the ventromedial neuropil (Ito et al 2014) in the ipsilateral central brain. The remaining three neurons are listed in Table 1 as TOpro2, TOpro3 and TOproX and probably belong to a group of cells which had earlier been summarized as L4-cells by Berger (1985).…”

“…We assume that one of them ramifies in layer 1 and the other potentially at the surface of layer 2. Neurons with ramifications in ALO-V layer 3 (Rosner et al 2017;Yamawaki 2019) sometimes had two fans and we assume that layer 3 actually consists of two layers of which we call the most proximal one layer 4…”

Target tracking behaviour of the praying mantisSphrodromantis lineola(Linnaeus) is driven by looming-type motion-detectors

“…The mantises clearly still identified our target as prey 662 rather than predator because they struck at it and never showed defensive behaviour 663 (Yamawaki, 2011). Yamawaki, 2019) and the responses of at least one of them (TOproL), are also 707 suppressed by WFM of a striped grating (Yamawaki, 2019). TOproM also gave larger 708 responses to looming verses receding stimuli although its firing rate did not increase 709 as the object approached, suggesting that TOproM was more sensitive to translating 710 objects rather than looming objects but clearly has looming-type sensitivities.…”

“…423and at an angular size responded to by target-selective selective neurons of the in the 424 lobula complex of the mantis Tenodera aridifolia(Yamawaki, 2019; Yamawaki and 425 Toh, 2003) as shown in Figure 3 A of Yamawaki and Toh (2003). In our experiments 426 motion of the target had a maximum speed of 209° s -1 , which is within 20% of the 427 highest contrast sensitivity of the mantis optomotor response (Nityananda et al, 2015) 428 and close to the angular velocity giving maximum response, of target-selective 429 neurons of the mantis Tenodera aridifolia to dark moving squares (Yamawaki and Toh, 430 2003) as in Figure 3 B in Yamawaki and Toh (2003).…”

“…TOpro M and L, like most looming neurons are not in themselves directionally selective 712 for the direction of target translatory motion(Yamawaki, 2019). Potentially their output 713 could be compared on the left and right side to allow directional responses as in the 714 locust(Yue et al, 2010).…”