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OlfactionIntegration of Sensory

Intrinsic State

Whole AnimalPerception

Hairs

Muscle Receptor Organ(Proprioception)

Publications related to sensory systems form our laboratory

Background of SENSORY SYSTEMS related to our research interests

The research goals related to sensory systems of my program are focused on understanding thephysiological mechanisms of development and plasticity among sensory systems. Mine is amultifaceted approach from studying differences in ion channels on the surface of membranes to theneuromodulatory molecules whose actions on sensory systems are relevant to the whole animal.Recent research from a physiological perspective has demonstrated the mediating role of hormones,neural circuitry, and their interactions in generating individualistic and social behavior, though relativelylittle attention has been given to the key contributions of sensory systems and the autonomic nervoussystem.

At a social level, animals show distinct differences in behavior and in responses to sensory cues. Forexample, among human siblings there may be dominant, outgoing individuals as well as shy andintroverted ones; some individuals learn new tasks better and quicker than others. The focus of muchresearch in this broad area has been on the central nervous system and has recently expanded intostudies of the expression of particular genes in the nervous system, in a variety of animal species. Thehope is to be able to get a handle on the mechanisms of how neurons are activated or turned off andhow they communicate with each other to elicit particular responses.

Such research in higher animals has proven to be a daunting task and many of the breakthroughs inneuroscience have arisen due to understanding of basic principles in simpler systems and thenextrapolating to more highly evolved organisms, such as humans. The invertebrate arthropods havelong provided key models, especially crayfish and Drosophila (T.H. Huxley, The Crayfish.1880; T.H.Morgan, 1900) for investigating neurophysiological principles. One advantage of invertebrates is thatindividual cells can be examined by a range of techniques from anatomical analysis to moleculargenetics and electrophysiology, to obtain insights that are not possible, at present, in higher-animalmodel systems. In particular, the sensory neurons of crayfish and Drosophila serve as models toinvestigate the basics principles of neuronal function which is relevant to all neurons in all animals.Combining the physiological and behavioral perspectives in addressing these issues holds muchpromise for significant progress in the field.

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Altered states of excitability of sensoryneurons : Proprioceptors

The effects of invertebrate hormones serotonin (5-HT) and ecdysone (20-HE) on primary sensoryneurons have only briefly been addressed in the literature. No reports to date have appeared on theeffects of 20-HE in relation to non-genomic, rapid influences on invertebrate sensory systems. Todetermine the effects of 5-HT and 20-HE on a identified sensory cell neuron, we chose to use theabdominal proprioceptive sensory system of crayfish, referred to as the muscle receptor organs(MROs), which monitor the positions and movements of the abdominal segments (Eckert, 1961;McCarthy and MacMillan, 1995). This mechanoreceptor transduces the stimulus of stretch of thesensory endings into a receptor potential that is conducted past the cell body. If this potential exceedsa threshold, an action potential will result at the axon base.

The neuron cell body is located in close proximity to the muscle it monitors. Two distinct types ofstretch receptors exist in this sensory system--a slowly-adapting and a rapidly-adapting receptor. Theactivity pattern of the slowly-adapting MRO is dependent on the strength of the mechanical stretch.This MRO system in the crayfish is analogous to the intrafusal muscle spindle in mammals. However,the muscle spindle organs in vertebrates are challenging to investigate electrophysiologically, whereasthe sensory neurons of the MRO are easily accessible to extracellular and intracellular electrodes forlong term recordings. The cell bodies of the sensory neurons are relatively large (50-100 m indiameter) and not contained in a ganglion as in vertebrates. The excised preparation also allows easyapplication and access of various neuromodulators to the neurons to examine potential effects. Thenatural flexion of the segments within the intact crayfish abdomen can be mimicked in an excisedpreparation examined in a dish containing a physiological saline.

The MRO of the crayfish is a model sensory system that has been extensively studied for its basicproperties since its description in lobsters by Alexandrowicz in 1951. This preparation has served wellin understanding sensory transduction in general by the activation of stretch activated channels(Erxleben, 1989). In addition, voltage-clamp and patch-clamp studies of the neuronal membrane haveprovided a fundamental understanding of ionic flow, channel distribution and density to regionalproperties of sensory neurons in general (Brown et al., 1978; Edwards et al., 1981; Erxleben, 1989; Huntet al, 1978; Rydqvist and Purali, 1991; Rydqvist and Swerup, 1991; Purali and Rydqvist, 1992).

From these past studies the localized region termed the site of spike initiation was identified whichrelated to a region of reduced threshold to activation. The early work of Eckert (1961) had illustratedthat activation of the MRO in one abdominal segment can influence the activity of primary sensoryneurons in an adjoining segment. This revealed processing within the segmental ganglion and influenceof efferent control within the ventral nerve cord.

We are examining both the chronic and the acute effects of 5-HT and 20-HE upon this primary sensoryneuron by examining the changes in firing frequency in response to a static stretch, characteristic ofthe relatively inactive periods of movement observed for crayfish in their natural settings. We were alsointerested to know if the effects of the neuromodulators are dependent on the state of firing activity ofthe cell. These two points are fundamental to understanding sensory physiology and have not beenwell-addressed in mammalian or in invertebrate systems in respect to neuromodulation.


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Altered states of excitability of sensoryneurons:

Cuticular sensory hairs

This study illustrates the importance of determining the sensory contribution to the intrinsic activity ofmotor neurons, and demonstrates that 5-HT modulates not only the motor neurons but also sensoryinput to the pathway. This abdominal superficial flexor preparation in the crayfish allows one to addressissues fundamental to all circuits and chemical synapses.

Experiments were designed to assess the role of 5-HT in altering the activity of the sensory neuronswhich drive the motor neurons. Since the sensory axons are very small (1 to 10 m) and difficult tomonitor over time while changing the bathing medium, the entire distal 2nd root was monitored after itwas transected from the ganglia. In the presence of 5-HT, there was an increase in the frequency ofprimary sensory neurons upon stimulation of the cuticle. This indicates that incoming information to theVNC is enhanced by 5-HT. For this paradigm, activity frequencies were quantified for one secondimmediately before the simulation and for the first second of stimulation in both saline and 5-HT. Inthree of the six preparations there was an enhancement of sensory neuron activity upon exposure to5-HT without cuticular stimulation.

From these studies we have shown that 5-HT even enhanced the sensory input that drives the flexormotor neurons (Strawn et al., 2000).

Altered states of excitability in integration ofsensory information

The drive of the motor neurons can readily be examined by stimulation of various known sensoryneurons, which enables one to assess their role in altering motor neuron activity. In addition, theintegration of sensory information in the ventral nerve cord (VNC) which effects the motor output isaccessible for study in the crayfish. Thus, the crustacean nervous system enables one to investigateeach component of a sensory-ganglia-motor neuron-muscle pathway which elicits that behavior.

In lobsters and crayfish, it has been shown that injections of serotonin (5-HT) into the circulatorysystem cause the animals to assume a semi-dominant posture (a raised extension of the chelipeds,although with a flexed state of their abdomen. Livingstone et al., 1980). The actions of 5-HT in elicitingthese behaviors were shown to be selective within the VNC to enhance excitation of excitatory flexormotor neurons and decrease excitation of the inhibitor flexor motor neurons. Previous investigationsdid not address whether sensory neuron activity could be altered by 5-HT, and whether the alterationsin sensory neuron activity could have an effect on the activity of the superficial motor neurons. It is wellestablished in the Aplysia nervous system that 5-HT sensitizes a gill-withdrawal reflex (Siegelbaum etal., 1982) and it appears from the results presented herein in the crayfish system that 5-HT can alsoenhance sensory drive.


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The aims of this study were to examine the role of 5-HT on each component within a crayfish `sensory-ganglia-motor nerve-muscle' consisting of specific, identified cells within the second abdominalsegment. This study illustrates the importance of determining the sensory contribution to the intrinsicactivity of motor neurons, and demonstrates that 5-HT modulates not only the motor neurons but alsosensory input to the pathway.

We have shown that 5-HT enhances the motor drive in the presence of a given amount of sensorystimulation. Thus it appears that 5-HT alters the degree of integration of sensory input within theventral nerve cord of the crayfish (Strawn et al., 2000).

Aesthetasc sensilla on the antennules

Olfactory sense

A great photo from Dr. Thomas Breithaupt

Neural activity is widely recognized as a contributing factor for appropriate neural development in avariety of animal species. The pioneering work of Wiesel and Hubel (1963) toward understanding thedevelopment of the visual system affected by the presence and absence of visual stimuli demonstrateshow gross morphological alterations occur in synaptic organization in the various parts of the brainrelated to vision in cats. In a troglobitic (obligatory cave dwelling) crayfish species, it is known thatthese animals retain eye stalk musculature and reflexive eye movements such as: protective eyewithdrawal, geotactic eye stabilization as well as proprioceptive nystagmus. The blind cave crayfishused in our study normally inhabit a cave environment containing water either as streams or pools inwhich no light is present. The blind cave crayfish, Orconectes australis packardi Rhoades haveelongated antennae as compared to sighted crayfish. It is likely that this morphological characteristic ofthe crayfish is an adaptive trait for life in a cave. Past studies using the troglomorphic traits ofelongated antennae and reduced eyes of the amphipod crustacean Gammarus minus have shown thatthese traits are genetically determined and that natural selection may be responsible for their evolution(Culver et al., 1995).

Since the cave crayfish have a reduced visual system, it would not be surprising either tactile and/orchemosensory systems are enhanced. Detailed developmental studies in tracing olfactory afferentprojections from the antennular nerve to the olfactory lobe, in the central brain, and interneuronsprojecting from the olfactory lobe to ganglia in the eye stalk have recently been undertaken (Schmidt,1997; Harzsch et al., 1997). The olfactory projection neurons (OPN) have their cell bodies within theolfactory lobe and send their axonal projections, via the olfactory globular tract (OGT) to hemiellipsoidbodies in the eye stalk ganglion (Schmidt, 1997; Harzsch et al., 1997). The OGT forms a distinctsub-group of small axons within a region in the protocerebral tract. The protocerebral tract is the nervebundle of the eye stalk that contains the axons to and from the ganglia within the eye stalk and thecentral brain, formally referred to as the optic nerve (Schmidt, 1997; Sandeman et al., 1998;Nunnemacher and Davis, 1966; Wiersma and Yamaguchi, 1966). The OPN bundle, has been identified incross sections of the protocerebral tract within the shore crab, Carcinus maenas (Schmidt, 1997).

We have already demonstrated that the cave crayfish have many more second order neurons dedicatedto chemosensory information as compared to epigean (surface) crayfish (Cooper et al., 2001), but morestudies are needed for a broader comparative investigation.

Our purpose is to compare morphological differences of the chemosensory structures of surface and


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troglobitic crayfish. We have started counting the number of aesthetasc sensilla on the antennules ofvarious crayfish and have very encouraging results to date. There are also a number of crayfishspecies across the state of KY that are housed in a collection museum at EKU under the directorship ofDr. Schuster. Dr. Schuster is a world authority on crayfish life history and their biology. This work willbe done in collaboration with Dr. Guenter Schuster at EKU.

This research topic raises an issue of environmental concern on water quality, particularly for cavecrayfish which do not have an option to make use of visual cues. What impact would chemicalpollutants have in the ability of the animals to detect important pheromone signals for reproduction ?Or maybe even predator detection? These questions are now being tackled using epigean (surfacedwelling) crayfish in order to postulate the potential threats to cave crayfish as well as othercave-adapted organisms.

With the recent developmental plans of airports, truck depots and highways over extremely biologicaland geological fragile areas such as in the karst plans of western Kentucky (in the vicinity of Mammothcave) the effects of toxic chemical will unfortunately directly test their impact on the survival of manycave-dwelling and troglobitic species. We will be working to continually survey the impact on the caveecosystems in relation to altered olfactory communication.

Whole animal perception

As with all crustaceans investigated, crayfish are very much aware of their surroundings and react toeven the slightest of disturbances. No where is this more apparent in a still, shallow pool of water withina cave in which the slightest vibration will set off ripples traveling through the water which will quicklybe monitored by the elongated antenna of a crayfish. What will determine if the crayfish flees or waits ?Is it the strength of the stimulus or interval at which they occur? Or maybe differences in an individualsphysiological state will determine if the animal will flee or fight it out. These are the types of questionsthat we are tackling to answer. In order to better understand what external and internal factorsinfluence the animals behavior one has to know the types of senses the animal possess and the rangein sensitivity of these senses. One might casually think that since a particularly troglobitic crayfish doesnot contain pigment in their eye caps or even rudimentary sensory structures in the eye that they arenot sensitive to light, however this is a misconception. The blind cave crayfish are responsive to lightby a photo receptor that is within their nerve cord contained in the tail. They can not see with this photoreceptor but they can detect if white light is shining on them. We recently have demonstrated that whitelight does alter the types social interactions that normally occur with cave crayfish (Li and Cooper,2002). We have also shown that red light or IR light does not cause any physiological changes in heartrate (HR) and ventilatory rates (VR), however exposure to white light dramatically alters both HR and VR(Li et al., 2001). In addition we have shown that the duration of social contact is decreases among twocrayfish when they encounter each other in the presence of white light. Thus, long term consequencesmight even alter reproductive success and ultimately the population of the species.

What is so nice by monitoring HR and VR in the relatively rare cave crayfish is that it is non-lifethreatening. Two little sterile wires are placed just under the cuticle on the back of the crayfish andwhen the recording is over the wires can either be removed or just cut off close to the cuticle so thatwhen the animal molts the ends of the wires are shed along with the old exoskeleton.

Since working in the field within the various caves has proven to be difficult, we remove crayfish fromthe cave environments to retain them in a cave-like environment within our laboratory at the Universityof Kentucky. This serves many useful purposes since within defined environmental conditions we canexclude various environmental cues such as olfactory signals which alter how the crayfish respond tovarious stimuli. In addition, we can add specific cues and examine their influence on individual andsocial behavior.

These studies had demonstrated that HR & VR represents a functional state that relate to


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environmental changes, thus allowing one to index an autonomic state of the animal (Listerman et al.,2000; Li et al., 2000; Schapker et al., 2001). The responses in crustaceans to environmentaldisturbances are similar to those of vertebrates that are regulated by autonomic control. The purposeof our study is to determine if simultaneous measures of HR and VR may serve as good biologicalindices to use in crayfish to assess if an animal is sensitive to alterations in its environment duringwhich time behavioral observation would not be as favorable for assessment. In addition, we wanted toknow if measures of HR and VR would provide insight into the function of the autonomic state ofcrayfish prior and during agonistic encounters.

Influence of animals intrinsic state

Prey use several tactics in order to evade predators. These include hiding, being motionless, or rapidlyescaping. For instance, crayfish have developed the tail flip to escape the predation of birds, fish,reptiles, and other crayfish. Different responses are utilized for different threats and these responsesmay change as the animal grows. How animals respond to various sensory stimuli during differentdevelopmental stages of their life depends on many factors. For example, smaller crayfish are morelikely to tail flip during an encounter with a larger crayfish (Pavey and Fielder, 1996), and experienceplays a role in determining this behavior (Copp, 1986). Also, responses to various stimuli depend on thesensing acuity of an animal. Much of our understanding of sensory systems is derived from examiningindividual sensory systems isolated from the organism as a whole (Atema et al., 1988). Approaching thesituation in this manner does not accomplish the ultimate goal of understanding the animals behavior(Atema et al., 1988; Burmistrov and Shuranova, 1996; Zulandt-Schneider et al., 1999).

The evolutionary changes observed in blind cave crayfish suggest the importance of nervous systemplasticity in promoting the survival of the species. In addition to providing a good comparison for blindcave crayfish, sighted crayfish make a good model for further exploring the sensory system involved inthe tail flip response. In most animals, the dissection of individual neurons and neural circuits tounderstand the complex integration of sensory and motor systems is extremely challenging. Crayfishserve well as a model organism for investigating escape behaviors. They have evolved particularbehaviors that can be quantified and investigated even at the level of neural circuitry. For example, thetail flip response in relation to the age of the animal and the size of the neurons with the circuit havebeen examined (Fricke, 86). Furthermore, the sensory difference in a blind cave crayfish (Orconectesaustralis packardi) suggests that they might have evolved a different responsiveness to tailfliping inrelation to the developmental stages. It seems reasonable that the blind cave crayfish do not have theadvantage of responding to visual stimuli through various neuronal circuits to elicit a tailflip as duesighted crayfish. On the other hand, it is assumed that the blind cave crayfish rely heavily on their othersenses to meet the challenges of cave life in total darkness (Barr and Holsinger, 85; Culver et al., 95).These unique adaptations may show differences in the habituation of the crayfish due to changes in theanimals sensory state.

Comparing the blind cave crayfish responses with previous studies on sighted crayfish provides insightinto the factors that drive selection for the tailflipping behavior. Previous studies dealt with the tail flipresponse being advantageous to the animal at various stages of its life. Juvenile, sighted crayfish aremore likely to respond to threatening stimuli by tailflipping, while adult crayfish are more likely torespond with the defensive use of their chelipeds. Fricke (1986) noted that the chelipeds of the juvenilecrayfish account for little of the animals total body mass when compared to that of an adult. Thus,juveniles can tail flip without the energy cost of moving the large mass of the cheliped. Morphologically,the thinner exoskeleton of small crayfish makes them less able to withstand the stress of predation.Consequently, they may have evolved greater tailflipping capabilities. Mature adults of Procambarusclarkii will not exhibit tailflips when both of their chelipeds are intact, and it has been suggested that thedisproportionate development of cheliped mass to body mass of the animals does not favor tail flippingin adults (Fricke, 1986). We have shown that O. a. packardi exhibit even greater ration of cheliped


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length to body length. Yet, a much higher occurrence of tail flipping exists in adult cave crayfish thanfor adults of P. clarkii. Conclusively, tail flipping behavior differences among species of crayfish is notjust a function of body proportions. The blind cave crayfishs sensory state may be an additional factorin generating tail flipping behavior.

Another facet, the neural circuitry of the tailflip response, has been examined extensively (Krasne andWine,1975; Olsen et al., 1996; Yeh et al., 1997; Krasne et al., 1997). Krasne and Wine (1975) identifiedthree pathways crayfish use to elicit a tailflip response: lateral giant, medial giant, and non-giant.Krasne and Wine (1975) used touches on the tail in order to elicit lateral giant responses. They initiatedfurther studies of the neural circuitry by eliciting lateral giant responses to drive the tail flip behavior.Subsequently, Fricke (1986) noted that stimuli given every 30 seconds caused intermediate sized (>10cm) crayfish to show habituation. The same protocol used on smaller individuals elicited habituationresistant behavior. Later, a physiological explanation was proposed by Edwards et al. (1994). As acrayfish grows, there is an increasing predominance of the depression-prone synapses in carryinginformation from the sensory neurons. These results demonstrate that larger animals have a faster rateof habituation than do smaller ones.

A link has been established between claw removal and the tendency to increase tailflips generated bymedial and non-giant pathways (Krasne and Wine, 1975; Lang et al., 1977). These previous studies haveexamined modulation of the crayfish tail flip response over long periods of time; however, they have notexamined the habituation of the tailflip response for possible modulatory influences over a short termbasis (i.e., seconds). It seems reasonable that the survival of the crayfish would be aided by the abilityto modulate the tail flip response. Change within short periods of time and to a variety of factors wouldpromote crayfish survival. The tailflip response could be modulated from direct neural input within thecircuitry and/or by release of neuromodulators form gain setting neurons.

To examine habituation rates in the tail flip response based on size of P. clarkii, three distinct sizegroups were tested. The group of large individuals consisted of the largest adults commonly found inthe field (Raceland, LA). The size of small crayfish compares to earlier reports on habituation of tail flipresponse (Fricke, 86). Small crayfish were the same size as the adult cave crayfish used in this study.The intermediate-sized group of P. clarkii provided a third grouping to determine a size relationship inthe habituation response.

This study demonstrates that the probability of the crayfish, P. clarkii, to tailflip in response to a touchon the dorsal tail fan is dependent on the size of the animal and the behavioral state of the animal(Kellie et al., 2001). The larger the animal, the less likely it is to tailflip. Also, a size dependency for anincreased tendency for exhibiting habituation to the stimuli with repetitive trials exists. Altering theanimals physical state by autotomizing the chelipeds increases the tailflip response in larger animals.Altering the environment, such as to one with little water depth, also can cause crayfish to responddifferently to the stimulus. For example, small crayfish will habituate more rapidly when placed inshallow water. Observations of adult crayfish of a species adapted to live in cave darkness revealedthat they are more likely to tailflip than sighted adults of a different species. When the troglobiticcrayfish were examined within a group, they exhibited a decrease in general movement over time. Thus,interaction instances decreased. However, the probability to tailflip remained constant in spite of thedecrease in interactions.

Publications related to sensory systems form our laboratory

Listerman, L., Deskins, J., Bradacs, H., and Cooper, R.L. (2000) Measures of heart rate during socialinteractions in crayfish and effects of 5-HT. Comparative Biochemistry and Physiology A.125:251-264(Listerman and Deskins were undergraduates in my laboratory at UK, Bradacs is collaborator fromAustria).

Li, H., Listerman, L., Doshi, D., and Cooper, R.L. (2000) Use of heart rate to measure intrinsic state ofblind cave crayfish during social interactions. Comparative Biochemistry and Physiology A.127:55-70.(Listerman and Deskins were undergraduates in my laboratory at UK).

Strawn, J.R., Neckameyer, W.S., and Cooper, R.L. (2000) The effects of 5-HT on sensory neurons, CNScommand, and neuromuscular junctions of the crayfish abdominal superficial flexor. ComparativeBiochemistry and Physiology B 127:533-550.(Strawn is an undergraduate in my laboratory at UK, Dr. Neckameyer is a collaborator in St. Louis).

Cooper, R.L., Li, H., Long, L.Y., Cole, J., and Hopper, H.L. (2001) Anatomical comparisons of neural


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systems in sighted epigean & troglobitic crayfish species Journal of Crustacean Biology 21:360-374.(Li is my PhD student, Long (Lis wife) helped out in axon counting, Cole and Hopper helped withassessing the cave crayfish and conducting experiments within the cave environment).

Li, H. and Cooper, R.L. (2001) Spatial familiarity in the blind cave crayfish, Orconectes australispackardi. Crustaceana 74: 417-433. (Li was my PhD student).

Kellie, S., Greer, J. and Cooper, R.L. (2001) Alterations in habituation of the tail flip response in epigeanand troglobitic crayfish. Journal of Experimental Zoology 290:163-176.(Kellie and Greer were undergraduates in my laboratory at UK)

Li, H. and Cooper, R.L. (2002) The effect of ambient light on blind cave crayfish: Social interactions.Journal of Crustacean Biology 22:449-458 (Li was my PhD student).

Schapker, H., Breithaupt, T., Shuranova, Z., Burmistrov, Y. and Cooper, R.L. (2002) Heart rate andventilatory correlative measures in crayfish during environmental disturbances & social interactions.Comparative Biochemistry and Physiology A 131:397-407. [FullText.pdf].(Schapker was a undergraduate student in my lab at the Univ. of KY. Dr. Breithaupt is a faculty memberat the University of Konstanz, Germany. Drs. Shuranova and Burmistrov are a Russian husband andwife team that have been working on crayfish and other invertebrate behavior for over a half ofcentury).

Cooper, R.L., Ward, E., Braxton, R., Li, H., and Warren, W.M. (2003) The effects of serotonin andecdysone on primary sensory neurons in crayfish. Microscopy Research and Technique 60: 336-345.[PDF] (Ward, Braxton, and Warren were undergraduates and Li was a graduate student in mylaboratory).

Ziemba, R., Simpson, A., Hopper, R., and Cooper, R.L. (2003) Comparisons of aesthetasc sensilla on thelateral antennules between two epigean (surface) species and the blind cave crayfish Orconectesaustralis packardi. Crustaceana 76: 859-869. [PDF] (Anna Simpson was an undergraduate in mylaboratory at UK).

Shuranova, Z.P., Burmistrov, Y.M., and Cooper, R.L. (2003). A hundred years ago and now: A shortessay on the study of the crustacean hindgut. (Vor hundert Jahren und nun: Eine kurze Geschichte vondie Forschung des Hinterdarmes der Crustaceen). Crustaceana 76:755-670 [PDF].

Shuranova, Z.P., Burmistrov, Y.M., and Cooper, R.L. (2003). Activity of the ventilatory muscles in thecrayfish. Comparative Biochemistry and Physiology A. 134: 461-469 [PDF] (Drs. Shuranova andBurmistrov are a Russian husband and wife team and are collaborators).

Tilden, A.R., Brauch, R., Ball, R., Janze, A.M., Ghaffari, A.H., Sweeney, K., Yurek, J.C. and Cooper, R.L.(2003) Modulatory effects of melatonin on behavior, hemolymph metabolites, and neurotransmitterrelease in crayfish. Brain Research 992:252-262 [PDF]

Pag, M.-P. and Cooper, R.L. (2004) Novelty stress and reproductive state alters responsiveness tosensory stimuli and 5-HT neuromodulation. Comp. Biochem. Physiol. A 139:149-158 [PDF].

Shuranova, Z.P., Burmistrov, Y.M., Strawn, J.R., and Cooper, R.L. (2006). Evidence for an AutonomicNervous System in Decapod Crustaceans. International Journal of Zoological Research 2(3):242-283.[Full text PDF] color figures.

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