THE NEUROHORMONE SEROTONIN MODULATES the PERFORMANCE of a MECHNOSENSORY NEURON DURING TAIL POSITIONING in the CRAYFISH by HSING
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THE NEUROHORMONE SEROTONIN MODULATES THE PERFORMANCE OF A MECHNOSENSORY NEURON DURING TAIL POSITIONING IN THE CRAYFISH by HSING-JU TSAI Submitted in partial fulfillment of the requirements For the degree of Master of Science Thesis Adviser: Dr. Debra Wood Department of Biology CASE WESTERN RESERVE UNIVERSITY August, 2009 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of _____________________________________________________ candidate for the ______________________degree *. (signed)_______________________________________________ (chair of the committee) ________________________________________________ ________________________________________________ ________________________________________________ ________________________________________________ ________________________________________________ (date) _______________________ *We also certify that written approval has been obtained for any proprietary material contained therein. TABLE OF CONTENTS LIST OF FIGURES ...........................................................................................................2 LIST OF ABBREVIATIONS............................................................................................3 ABSTRACT ......................................................................................................................4 INTRODUCTION .............................................................................................................5 BACKGROUND................................................................................................................8 Muscle Receptor Organ..........................................................................................8 Crayfish Social Behavior......................................................................................12 Serotonin Actions as a Gain-Setter.......................................................................14 Serotonergic Neuromodulation and Crayfish Social Status..................................15 Neural circuits underlying social status plasticity.................................................17 METHODS........................................................................................................................19 RESULTS..........................................................................................................................25 DISCUSSION....................................................................................................................52 REFERENCE.....................................................................................................................60 1 LIST OF FIGURES Figure 1…………………………………………………………………………………9 Figure 2………………………………………………………………………………..10 Figure 3………………………………………………………………………………..26 Figure 4………………………………………………………………………………..28 Figure 5………………………………………………………………………………..29 Figure 6………………………………………………………………………………..30 Figure 7………………………………………………………………………………..32 Figure 8………………………………………………………………………………..34 Figure 9………………………………………………………………………………..36 Figure 10………………………………………………………………………………37 Figure 11………………………………………………………………………………40 Figure 12………………………………………………………………………………41 Figure 13………………………………………………………………………………42 Figure 14………………………………………………………………………………43 Figure 15………………………………………………………………………………44 Figure 16………………………………………………………………………………45 Figure 17………………………………………………………………………………46 Figure 18………………………………………………………………………………47 Figure 19………………………………………………………………………………48 Figure 20………………………………………………………………………………49 Figure 21………………………………………………………………………………50 2 LIST OF ABBREVIATIONS CNS Central Nervous System LG Lateral Giant Neuron MG Medial Giant Neuron MRO Muscle Receptor Organ N2 Nerve 2 SR1 Type 1 Sensory Receptor SR2 Type 2 Sensory Receptor 5-HT 5-hydroxytryptamine; Serotonin 3 The Neurohormone Serotonin Modulates the Performance of a Mechnosensory Neuron During Tail Positioning in the Crayfish Abstract by HSING-JU TSAI Neurohormones are known to provide adaptive flexibility in animal behavior. The type 1 sensory neuron (SR1) in the crayfish abdominal muscle receptor organ is thought to function in slow postural abdominal positioning. I tested the hypothesis that SR1 responds differently to serotonin depending upon the movement performed. The SR1 threshold response, its adaptation rate, and its dynamic range are influenced by serotonin. During cyclical abdominal movements that mimic swimming, the SR1 firing frequency is higher and the adaptation rate is lower than during sustained abdominal stretches. Generally, the response of a crayfish to the modulator serotonin depends upon its social status. Our preliminary data indicate that without serotonin, the dynamic range of SR1 suggests higher sensitivity to changes in abdominal position for socially isolated crayfish versus those with social experience. With serotonin, SR1 threshold properties appear to be different for subordinate crayfish and similar between dominants and isolates. 4 INTRODUCTION An essential task of the nervous system is to monitor external conditions to mediate changes in behavior. During ongoing movement, peripheral sensors send feedback to the central nervous system (CNS) that allows adaptive behavior under changing conditions (review in Pearson, 1993). Proprioceptors are neurons in the peripheral nervous system that provide feedback concerning the position of body parts. It has been demonstrated in many model systems that this feedback is integral to shaping the form of an ongoing behavior (Pearson, 2004). The activity of sensory neurons may also be mediated by the physiological state of an animal (Catteraert et al. 2002). The influence of peripheral receptors can be state-dependent, that is, the impact of sensory input may depend upon the motor pattern or behavior performed (Hultborn, 2001; Buschges and el Manira, 1998; Ausborn et al., 2007; Combes et al., 1999; Blitz et al., 2004; Hooper and Moulins, 1989). The activity of sensory neurons can be ‘modulated’ by numerous mechanisms including central pre-synaptic inhibition of these sensory afferents (Beenhakker et al., 2005; Wachowiak et al., 2002; Cattaert et al., 2002; Sillar and Skorupski, 1986; Wolf and Burrows, 1995; Dubuc et al.,1988; Gossard et al., 1989; Gossard, 1996; review in Torkkeli and Panek, 2002), input from other peripheral neurons (el Manira et al., 1991; Fabian-Fine et al., 1999, 2000; Panek et al., 2002; Pasztor and Bush, 1987), and changes in intrinsic membrane properties due to both local and hormonal neuromodulatory inputs (Hultborn, 2001; Kravitz, 1988; Rao and Hingerman, 1983). These mechanisms provide plasticity in proprioceptive input that may contribute to adaptive behavioral changes. 5 As an animal moves in its environment, multiple proprioceptive inputs from each limb and from the torso are activated. The volume and changing character of sensory information over time may be unnecessary for regulating ongoing behavior. Response adaptation to an ongoing stimulus is a feature of sensory neurons that allows information to be filtered such that only the most relevant input is available to the CNS (Wark et al. 2007). Sensory neurons may also be tuned to a range of stimulus intensities that are most effective for their activation. The threshold stimulus for response sets a limit for the range of a sensory neuron. Tuning to a dynamic response range is another feature that contributes to capture information that is most relevant. These features of proprioceptors can be modulated (Birmingham, 2001; Hultborn, 2001; Ramirea and Orchard, 1990; Orchard et al., 1993). The crayfish abdominal muscle receptor organ (MRO) is an example of a stretch activated proprioceptor (Fields, 1966; Page, 1982; Macmillan and Patullo, 2001). The MROs are activated by flexion or curling of the crayfish tail. The MROs contain two types of stretch receptor neurons (SR1 and 2) that are essential for motor control of the tail (Fields, 1976; Page, 1982; Macmillan, 2002). In most studies, SR1 is characterized as tonically active and slow-adapting and SR2 is phasically active and fast-adapting (Florey and Florey, 1955; Wiersma et al., 1953; Kuffler, 1954; Eyzaguirre and Kuffler, 1955a, b; Rydqvist et al., 2007; Cattaert and Le Ray, 2001). In most reports, SR1 receptors are studied in reduced preparations with slow and sustained stretch protocols (e.g. Fields, 1966; Cooper et al., 2003; Pastors and Macmillan, 1990). These studies were motivated by the idea that the SRs have a role in detecting slow changes in postural control of the tail (Fields, 1966; Page 1982). More recent studies using intact, freely behaving crayfish have indicated that SR1 also has a role in escape 6 swimming where tail movements are more rapid and less sustained than typical slow postural movement (McCarthy et al., 2004; Wine and Krasne, 1972, 1982; Fields, 1976). My hypothesis is that SR1 performance differs during postural and cyclical movements and that SR1 responds differently to the neurohormone serotonin (5-HT) depending upon the movement executed. The influences of the neurohormone 5-HT on crayfish behavior are best understood in the context of social behavior (review in Edwards and Kravitz, 1997). Crayfish form social hierarchies and have distinct behaviors according to social status (Bovbjerg, 1953, 1956; Lowe, 1956; Copp, 1986, review in Huber, 2005). Dominance relationships play a role in the competition for food, shelter, and mating; however, social status is highly plastic in crayfish (discussed in Goessmann et al., 2001; Peeke et al., 2000). Under appropriate