Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function

Abstract

IntroductionPlanarians belong to an evolutionarily early group of organisms that possess a central nervous system including a well-organized brain with a simple architecture but many types of neurons. Planarians display a number of behaviors, such as phototaxis and thermotaxis, in response to external stimuli, and it has been shown that various molecules and neural pathways in the brain are involved in controlling these behaviors. However, due to the lack of combinatorial assay methods, it remains obscure whether planarians possess higher brain functions, including integration in the brain, in which multiple signals coming from outside are coordinated and used in determining behavioral strategies.ResultsIn the present study, we designed chemotaxis and thigmotaxis/kinesis tracking assays to measure several planarian behaviors in addition to those measured by phototaxis and thermotaxis assays previously established by our group, and used these tests to analyze planarian chemotactic and thigmotactic/kinetic behaviors. We found that headless planarian body fragments and planarians that had specifically lost neural activity following regeneration-dependent conditional gene knockdown (Readyknock) of synaptotagmin in the brain lost both chemotactic and thigmotactic behaviors, suggesting that neural activity in the brain is required for the planarian's chemotactic and thigmotactic behaviors. Furthermore, we compared the strength of phototaxis, chemotaxis, thigmotaxis/kinesis, and thermotaxis by presenting simultaneous binary stimuli to planarians. We found that planarians showed a clear order of predominance of these behaviors. For example, when planarians were simultaneously exposed to 400 lux of light and a chemoattractant, they showed chemoattractive behavior irrespective of the direction of the light source, although exposure to light of this intensity alone induces evasive behavior away from the light source. In contrast, when the light intensity was increased to 800 or 1600 lux and the same dose of chemoattractant was presented, planarian behaviors were gradually shifted to negative phototaxis rather than chemoattraction. These results suggest that planarians may be capable of selecting behavioral strategies via the integration of discrete brain functions when exposed to multiple stimuli.ConclusionsThe planarian brain processes external signals received through the respective sensory neurons, thereby resulting in the production of appropriate behaviors. In addition, planarians can adjust behavioral features in response to stimulus conditions by integrating multiple external signals in the brain.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-014-0010-z) contains supplementary material, which is available to authorized users.

Activation of planarian TRPA1 by reactive oxygen species reveals a conserved mechanism for animal nociception

“…They are capable of active hunting behavior, and possess simple sensory systems 27,49 and a simple brain that operates using synaptic and neurotransmitter principles similar to those of the more complex insect or mammalian brains 50 .…”

“…The following fly strains were used: Canton-special, isogenic w 1118 (a gift from Marcus C. Stensmyr); elav-Gal4/CyO; trpA1 1 (BDSC#26504, backcrossed 5 times); 5xUAS-TRPA1-C (a gift from D. Tracey); tub-cyto-roGFP2-Orp1 49 . To generate UAS-SmedTRPA1 flies, Smed-TRPA1 cDNA (see above) was cloned into pCR™8/GW/TOPO® TA (Invitrogen) and then transferred into a 40xUAS destination vector created introducing the Gateway® cassette into pJFRC8-40XUAS- IVS-mCD8::GFP (Addgene #26221) via the XhoI/ XbaI restriction sites.…”

Girardia dorotocephala transcriptome sequence, assembly, and validation through characterization of piwi homologs and stem cell progeny markers

“…Planarians have also been the subject of recent work in toxicology, as well as behavioral, ecological, and evolutionary biology research (Alvarez-Presas et al, 2008; Hagstrom et al, 2016, 2015; Hicks et al, 2006; Inoue et al, 2015; Levin et al, 2016; Lombardo et al, 2011; Majdi et al, 2014; Shomrat and Levin, 2013), broadening their use as a model beyond fields related to developmental biology. In the classroom, these charismatic organisms have been an important component in K-12 science education and tools are being developed to modernize their use in college level courses (Accorsi et al, 2017; Eberhardt et al, 2015; Pagan et al, 2009; Valverde, 2015).…”

Planarian regeneration in space: Persistent anatomical, behavioral, and bacteriological changes induced by space travel

“…These bilaterians have the ability to completely recapitulate all body parts, including complex organs, from small pieces of the body, with high morphological and proportional fidelity (Hill & Petersen, ) in a vast variety of perturbations (Morgan, ). The complex organs include a full, centralized brain (Pagán, ; Sarnat, ) and central nervous system (Cebria, ) which has the ability to produce a continuous brain wave pattern (Aoki, Wake, Sasaki, & Agata, ) and complex behaviors (Corning, ; Inoue, Hoshino, Yamashita, Shimoyama, & Agata, ) with impressively variable sensory capabilities as inputs (Asano, Nakamura, Ishida, Azuma, & Shinozawa, ; Brown, , ; Brown & Park, ; Brown, Dustman, & Beck, ; Carpenter, Morita, & Best, ; Hyman, ; MacRae, ). Planaria exhibit complex learning, curiosity, and problem‐solving abilities (Best & Rubenstein, ; Corning & Freed, ; McConnell, ; Pagán, ; Wells, ).…”