Forgetting curve of cricket, Gryllus bimaculatus, derived by using serotonin hypothesis☆

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Abstract

It is thought that the adjustment of intraspecific aggression is an essential factor in the development of a social structure. To understand the natural laws for organizing the social structure, we focus on the fighting behavior of crickets, Gryllus bimaculatus, and investigate the neuronal mechanisms to adjust aggressiveness associated with a neuromodulatory biological amine: serotonin (5-HT).

In this paper, we present a working theory of a neurophysiological mechanism based on the past biological studies on the 5-HT hypothesis, and a mathematical model of the mechanism. We analyzed this model and concluded that this neurophysiological mechanism makes the forgetting process slower. Next, we fitted our theoretical forgetting curve to an experimental curve and estimated the parameters of our model. These estimated values were in agreement with common belief in biological science.

Highlights

► We proposed a neurophysiologic working theory for understanding of aggressiveness. ► We constructed a mathematical model of the theory described above. ► We analyzed it and found a physiological factor which slows the forgetting process. ► We suggested a biological experiment to confirm this finding.

Introduction

An ethologist has pointed out that the adjustment of intraspecific aggression is an essential factor in the development of a social structure [1]. Animals mediate their aggressiveness depending on social factors such as population density and external threats. The question arises, what kind of internal mechanism do animals possess to mediate their aggressiveness. In this study, we investigate the neuronal mechanisms in insects to mediate their aggressiveness and especially focus on the fighting behavior of crickets, Gryllus bimaculatus (Fig. 1). There are two reasons for selecting cricket. First, the different levels of a cricket’s fight can be clearly differentiated to observe behaviors [2]. Second, the body size of a cricket is large enough to carry out the neuropharmacological experiments. Thus, crickets are suitable for studying the mechanism of behavior neuromodulation.

The behavior of almost all insects is innate; this implies that there is a limit to the number of behavioral patterns, and therefore, insects can be said to have a behavior-based system. Therefore, insects must have the mechanism to modulate their behavior; they need to show a huge variety of behaviors against a huge variety of social structures for their survival. It has revealed that biochemical substances called neuromodulators, such as neuropeptide and biogenic amine, modulate behavior selection. It is known that crickets change their aggressiveness depending on the amount of biogenic amine: octopamine (OA) and serotonin (5-HT). OA and 5-HT are the neuromodulators that modulate aggressive behavior. It is also known that a fighting experience changes the amount of OA and 5-HT.

Once crickets lose in a fight, they avoid another fight for a prolonged time and recover their aggressiveness gradually [3]. The time evolution of behavior shift is called forgetting curve. Although this forgetting curve should be closely related to OA and 5-HT metabolism, an experimental result shows that the time constant of this forgetting rate is too small to be explained by a simple neurophysiological mechanism.

Kawabata et al. constructed a mathematical model of OA dynamics and succeeded in explaining the specific dynamics of a cricket group with their model [4]. In this paper, we present a working theory of a neurophysiological mechanism and a mathematical model based on past biological studies. For the verification of our model, we also derive another model by removing a specific factor from our model. For each model, we derive the intensity of behavior modulation and compare the time evolution of behavior with the observed time evolution (forgetting curve). We estimate the parameters of our model. Finally, we suggest a biological experiment and predict the result of this experiment.

Section snippets

Related works

A cricket shows fighting behavior in resource competition situations. When crickets find their opponent, they start fighting. Their aggression is modulated by the neuromodulators: OA and 5-HT [5], [6], [7], [8]. The neuromodulation process can be described as follows.

Crickets sense their opponent’s cuticular pheromone with their antennae [9]. The sensing of pheromones could lead to production of nitric oxide (NO) in the brain. NO activates soluble guanylyl cyclase (sGC) to generate cyclic GMP

Mathematical model construction

In this section, we construct a mathematical model on the basis of the 5-HT hypothesis and derive the intensity of behavior modulation from this model. Next, we derive its time evolution, which is equivalent to obtaining the forgetting curve. Third, we derive another forgetting curve by removing specific factors from the 5-HT hypothesis. Thus, we prepare two forgetting curves for comparative verification.

Analysis

To confirm whether or not the 5-HT system has autoreceptors, we estimate a major parameter by using two types of forgetting curves which are obtained as discussed above. Then, we compare this parameter with those obtained in past studies and make an assumption on the presence of an autoreceptor. Finally, we predict the time constant of 5-HT receptor internalization, which has never been measured for crickets.

Results

As shown in Fig. 7, the time constant of avoidance level 1 is about 60 min. Avoidance level 2 has two time constants: about 75 min and 43 h. In Fig. 7, we draw three curves. The broken line represents FS(t). The other two lines are fitting curves for 0–120 min data and 120–5660 min data.

During the interval 0–120 min, the effect of 5-HT recovery is dominant. We compare the theoretical prospect and fitting curve for 120–5660 min. The comparison shows that the model constructed by using 5-HT

Conclusions and discussions

We constructed a 5-HT system on the basis of the 5-HT hypothesis and estimated the time constant of the 5-HT receptor, b3, in crickets.

The time constant b3 has never been measured experimentally in crickets; the time constant, if available, can be used as a reference point to obtain the time constants associated with the 5-HT system for other animals. In this study, we use the 5-HT hypothesis that involves four time constants associated with the following dynamics:.

  • (1)

    Dynamics of vesicular

Acknowledgments

This work was partially supported by a Grant-in-Aid for Scientific Research on Priority Areas “Emergence of Adaptive Motor Function through Interaction between Body, Brain and Environment” from the Japanese Ministry of Education, Culture, Sports, Science and Technology, and supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science.

Shiro Yano received his B.S. in Science from Kyoto University in 2007 and M.S. in Engineering from the University of Tokyo in 2009. He is a JSPS Research Fellowship for Young Scientists. His research interest includes neuroethology, self-organizing system, affective disorder, and Mobiligence (Emergence of adaptive motor function through the body, brain and environment).

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      Based on the comparison to our previous work, we predicted to see reduced activity, boldness and aggression in manipulated crickets, and reduced exploration due to the observed link between the dopaminergic system and exploratory behaviour (Kempenaers et al., 2007). Mediterranean field crickets (Gryllus bimaculatus) were used because they are a model species for neuroethological studies (Horch et al., 2017; Yano et al., 2012), and display repeatable personality variation (Santostefano et al., 2016; Abbey-Lee et al., 2018). Further, using the same species as in our previous work on the effect of manipulation of monoamines on behaviour describing personality (Abbey-Lee et al., 2018), enabled to us to compare results obtained across studies.

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      Although flying or CDM treatment restores aggressiveness almost immediately, it cannot prevent the animals from losing in the first place [43], hence other mechanisms must be involved. A mathematical model for recovery from defeat has been developed for crickets from the assumption that serotonin is involved [73]. This amine is renown for its restraining effect on aggression in numerous animals including man [74].

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    Shiro Yano received his B.S. in Science from Kyoto University in 2007 and M.S. in Engineering from the University of Tokyo in 2009. He is a JSPS Research Fellowship for Young Scientists. His research interest includes neuroethology, self-organizing system, affective disorder, and Mobiligence (Emergence of adaptive motor function through the body, brain and environment).

    Yusuke Ikemoto received his B.S., M.S., and Dr. Eng in Engineering from Nagoya University, in 2001, 2003 and 2006, respectively. He was Research associate at The University of Tokyo and joined the Mobiligence program in the MEXT Grant-in-Aid for Scientific Research on Priority Areas from 2006 to 2010. At present, he is assistant professor of Dept. of Mechanical and Intellectual Systems Engineering, University of Toyama, Japan. His main research interests are distributed autonomous systems, intelligent robotic system, self-organizing system, bio-inspired robotic systems, and Mobiligence.

    Hitoshi Aonuma received the B.S., M.S., and Dr. Sci. degrees from the Faculty of Science, Hokkaido University, Hokkaido, Japan, in 1991, 1993, and 1998, respectively. From 1995 to 1996, he was with the Graduate School of Science, Hokkaido University, as a JSPS Research Fellow. In 1998, he was a Research Associate for BBSRC, School of Biological Sciences, University of Southampton, UK, where he was a JSPS Research Fellow from 1999 to 2000. From 2001 to 2003, he was an Assistant Professor, Research Institute for Electronic Science, Hokkaido University, where he has been an Associate Professor since 2003. His research interest includes neuroethology, neurobiology, and animal physiology.

    Hajime Asama received his B.S., M.S., and Dr. Eng in Engineering from the University of Tokyo, in 1982, 1984 and 1989, respectively. He was Research Associate, Research Scientist, and Senior Research Scientist in RIKEN (The Institute of Physical and Chemical Research, Japan) from 1986 to 2002. He became a professor of RACE (Research into Artifacts, Center for Engineering), the University of Tokyo in 2002, and a professor of School of Engineering, the University of Tokyo in 2009. He received JSME (Japan Society of Mechanical Engineers) Robotics and Mechatronics Division Academic Achievement Award in 2001, RSJ (Robotics Society of Japan) Best paper Award, JSME Robotics and Mechatronics Award in 2009, etc. He was an AdCom member of IEEE Robotics and Automation Society from 2007 to 2009, an editor of Journal of International Journal of Intelligent Service Robotics, Journal of Field Robotics, Journal of Robotics and Autonomous Systems, and Journal of Advanced Computational Intelligence and Intelligent Informatics. He played the director of the Mobiligence program in the MEXT Grant-in-Aid for Scientific Research on Priority Areas from 2005 to 2009. He is a Fellow of JSME since 2004 and RSJ since 2008. His main research interests are distributed autonomous robotic systems, ambient intelligence, service engineering, and Mobiligence.

    ☆

    Revised and extended version of a paper presented at the 3rd International Symposium on Mobiligence (Awaji, Japan, 2009).

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