command neurons in crustaceans

Comp. Biochvm. Ph).shd.. 1976. l ' l ,l 54A. 9P I to 5. Perffom,m Prcs~. Pelleted m (;real Britata

M I N I R E V I E W

C O M M A N D N E U R O N S IN CRUSTACEANS

ROnF.RT F. BOW'ERMAN AND JAMES L, LARIMER*

Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071, U.S.A. Department of Zoology, University of Texas at Austin, Austin, TX U.S.A.

(Received 24 February 1975)

HISTORICAL PERSPECrlVE

The command neuron concept was derived largely from the pioneering w o r k of Wiersma and co- workers. Among the earliest observations were those involving the giant fibers of crayfish. These large interneurons, termed the medial and lateral giant fibers, were shown to be capable of eliciting a form of escape behavior in these animals (Wiersma, 1938). Soon thereafter, small, more typical interneurons were localized in the circumesophageal connectives that were effective in accelerating and inhibiting the heartbeat of crustaceans (Wiersma & Novitski, 1942). A much 'more complex behavior, the defense reflex, readily recognized among the normal behavioral repertoire of the aninml, was shown to be evoked by stimulating other small interneurons in the circumesophageal connectives of crayfish (Wiersma, 1952). The term "command fiber", however, was first used to charac- terize the interneurons isolated from the abdominal nerve cord, which evoked various swimmeret movements (Wiersma & Ikeda, 1964). ' Work has since expanded and other preparations have been examined until we presently have substantial evidence for the existence of many types of command neurons. Thus the presence of identified cells capable of releasing organized segments of behavior were known to exist for some twenty years before they were examified in a wide variety of. preparations or before their full complement was appreciated,

SOME MODEL SYSTEMS FOR.COMMAND NEtmON RESEAaCH

Although the subsequent discussion will deal only with examples of command neurons from crustaceans, it is important to note that other preparations,, par- ticutarly the molluscs, offer some of the most interest- ing and well documented-systems of command or tt:igger cells. The brain of the nudibranch~ Tritonia gitberti, has been found to contain many' identifiable cells which, when stimulated, release:.various behaviors ranging from localized contractions'of branchial plumes to more complex movements such as turning, escape, and swimming (Willows, 1967). The. central origin and part of the undei'lying neural circuitry of the motor program for swimming was further illuci- dated by Dorsett et al. (1969), Willows et aL (1973)

* The research of the authors was supported by NIH grant NS-05423 (J.L.L.) and by NIH Fellowships NS-51. 05401 and GM 00836 (R.F.B.)

(.H.t ' . I ,~I 54 1,~, •

and Dorsett er al. (1973). Commands controlling gill movements have been found in Aplysia tPeretz, 1969). as well as those for gill and siphon movements (Kup- fermann et al., 1971; Kupfermann et al., 1974), while other central neurons are identified for the control of circulation, (Koester et al., 1974). Commands are also described for radular control in the snail Heft- soma (Kater & Rowell, 1973), and this list is not exhaustive.

Few if any identified command cells are known for insects, however, there are strong indications of their presence. For example localized brain stimulation has long been known to elicit singing behavior in Orthop- terans (Huber, 1962, 1967). Other commands are described for initiating flight (Wilson, 1961 : Mulloney, 1969) and for spiracle ventilation control (Miller, 1967, 1971) to cite a few. These and other examples, particularly those taken from invertebrate preparations Suggest that a uniqu e class 0f interneurons, each capable of triggering a recol~fizable behavior,

is widespread in the nervous systems of many organisms. More general 'treatments of command neurons in these and other preparations can be found in the following references: (Maynard, 1973; Kennedy er ak, 1969; Konishi, 1971; Kennedy, !971 ; Kennedy & Davis, 1975).

SINGLE NEURONS CAN RELEASE, BEHAVIOR

Ariy doubt that command neurons can be Single cells was dispelled early by several experiments. Ken- nedy and his co-workers (Kennedy et al., 1966) were able to secure, recording and stimulating access to both ends of the axons of command interneurofis for flexion and extension of the crayfish abdomen. Only when impulses were .seen in the command neurons was the behavior released, and this held for both abdominal flexi0n and extension commands. In another case it was shown that by recording down .stream from the"site of'stimulat!on, a single impulse train, presumably that of the command element, could 'be directly corrdated with the driven behavior, in this case, .a cyclical movement of the uropods (Larimer & Kennedy, 1969b). Stimulation of individual lateral and medial giant fibei's have likewise shown that" single cells can elicit complete yet different behaviors (Larimer et al., 1971). These and similar experiments with molluscs therefore leave little doubt that singl6 neurons can underlie" relatively Simple behaviors, however,- such data can only be inferred for the complex commands (Bowerman & Latimer, 1974a, b).

2 R o ~ R T F. BoWERMAM AND JAM~.S L. LARIMER

CHARACTERISTICS OF COMMAND ELEMENTS Command neurons have been studied primarily by

dissecting out fine bundles of axons from various connectives of the CNS. Unpatterned stimuli are gener- ally used to drive the units, while observing either the motor neuron discharge pattern or the evoked behavior. Although several overt characteristics of command systems can be.observed this way, only a few generalizations about their structure and organization have emerged. Researchers utilizing crustacean models have studied primarily the command elements in the abdominal cord which affect abdominal positioning (Evoy & Kennedy, 1967; Evoy, 1967; Kennedy et aL, 1966; Kennedy et al., 1967) and swimmeret control (Hughes & Wiersma, 1960; Wiersma & Ikeda, 1964; Stein, 1971; Davis & Kennedy, 1972a, b,c); however work has also been done on the uropod movements (Larimer & Kennedy, 1969a, b) stomach and intestinal movements (Dando & Selverston, 1972; Winlow & Laverack, 1972; Wolfe & Larimer, 1971; Wolfe, 1973) and on cardiac and ventilation control (Wiersma & Novitski, 1942; Wilkens et al., 1974; Field & Larimer, 1975). Reports on the command neurons emerging from the brain (Atwood & Wiersma, 1967; Bowerman & Larimer, 1974a, b) have demonstrated that extremely complex behaviors, as well as simpler movements, Can be evoked at that level.

Many of the principles of command fiber activity were obtained from the work on abdominal positioning and swimmeret control where simpler commands are typical mxd detailed motor neuron outputs are accessible. It was shown by Kennedy & Takeda (1965b) that slow tonic abdominal flexion is controlled via only 10 motor neurons and two inhibitors per abdominal segment. Similarly, tonic extension is" controlled by the same number of motor and inhibitor nerves. Thus, all possible positions of the abdomen can be achieved through activity of only 20 motor neurons and four peripheral inhibitors per segment. Most importantly , each motor neuron and inhibitor can be identified from its firing pattern and characteristic spike amplitude. With this access to motor outflow it was possible to observe the output of individual flexion and extension commands in detail. Corresponding accounts of the motor output of the sixth ganglion in crayfish (Larimer & Kennedy, 1969a) and of the swimmeret motor neurons of lobsters (Davis, 1968, 1969; Davis & Kennedy, 1972a) allowed an extension of the analysis to more complex and cyclical behaviors.

Various studies have established that command fibers release their behaviors when driven at frequen- cies within the "normal" range, i.e. between 10 and 100Hz. There is often a frequency threshold (Wiersma & Ikeda, 1964; Evoy & Kennedy, 1967) as well as a strong frequency dependence of the output (Evoy & Kennedy, 1967; Davis & Kennedy, 19720; Dondo & Selverston, 1972). In the extreme ease, Atwood & Wiersma (1967) observed that complex behaviors evoked by a single command changed dramatically with input frequency. For example, at 2 Hz the 5th pereiopods rotated backwards, but at 4 Hz several events emerged in addition, indudin5 backward movement of swimmerets, abdominal fir.x- ion and telson extension. At 10 Hz a defense ref,~ex

appeared and at 15--20Hz there was a less specific "struggle" response. Finally, wizen stimulated repeat- edly or for prolonged periods, most command elements lose their effectiveness (Evoy & Kennedy, 1967; Latimer & Kennedy, 1969b; Latimer et at., 1971). The nature of this "'adaptation" in the small fibers is not known, however, it has some symptoms, of habituation, others of fatigue. The relatively simple escape response due to lateral giant activity also subsides with an habituation. In this case, however, habituation has been shown to be due to antifacilitation of the chemical synapses between the receptors and tactile interneurons in the circuit (Krasne, !969; Zucker. 1972b).

Questions concerning the number of command elements that might exist within a crustacean nervous system cannot yet be answered, however, sufficient data exist to make certain generalizations. A few examples of the number of elemet~'.s encountered are as follows. In the crayfish, some five exeitors and at least three inhibitors were found to influence the swimmeret rhythm (Wiersma & Ikeda, 1964). It was estimated that there are perhaps fewer than 20 each of command fibers involved in flexion or extension in the crayfish abdominal connectives (Evoy & Ken- nedy, 1967). About 15 command fibers were found in the crab Cancer nmoistes which affected heart rate and ventilation (Wilkens et aL, 1974) and some 10 accelerator and 14 inhibitory units were found in each circumesophageal connective that influence the heartbeat in crayfish (Field & Larimer, 1975L Only two commands, however, have been reported that affect the gastric and pyloric rhythm of the foregut of spiny lobsters (Dando & Selverston, 1972). In the more complex responses, five neurons were found which evoked forward walking and four that caused backward walking, while four. released swimming and escape (exclusive of giant fibers) (Bowerman & Lar- liner, 1974b). Although classed as flexion, extension, swimmeret, walking, swimming etc. there has been little if any redundancy observed among the different neurons, instead, each unit seems to evoke a unique behavior or a recognizable part of a behavior. This latter aspect has led to the concept that many command elements must operate in concert to achieve a recognizable behavior (Larimer & Kennedy, 1969b; Davis & Kennedy, 1972a). Others, however, are apparently capable of singly releasing rather complex yet unique behaviors (Atwood & Wiersma, 1967; Bowerman & Latimer, 197am, b).

The systematic search for command elements has demonstrated too that it is possible to isolate the same unit from the oame area of the connective in different individuals qZ,,t~s its location is characteristic and the motor prog.'am or behavior that is evoked is apparently identical from individual t o individual within a species. Such data strongly suggest a genetic specification of large segments of the nervous system of these animals. The size of the specified network would vary according to the complexity of activity evoked by the command neuron in question. For example, in the case ofcommands for simple abdominal flexion, only one or a few segments might be in- vob,'ed, with perhaps 40-60 motor neurons activated (Evoy & Kennedy, 1967; Evoy et aL, 1967). The associated circuitry between the command element and

C o m l l l a n d net l rol ls ill c r u s t a c e a n s 3

the motor neurons is unknown in this case, but could perhaps comprise as few as 20 other cells. Even here the specified synaptic connections must number in the thousands. Swimmeret commands elteet the motor neurons controlling the 12 muscles/limb (Davis, 1968) and as many as five pairs can be activated. Although each limb or pair of limbs may perform essentially the same movement, they must be placed in meta- chonal order (Stein, 1971). Thus the number of specified connections in this case must be even larger. If one considers the most complex commands, e.g. defense responses (Atwood & Wiersma, 1967; Bower- man & Larimer, 1974a) or forward walking (Bower- man & Larimer, 1974b) then thousands of neurons must cooperate at all levels of the CNS. An additional principle of command elements which is now well documented is that of pattern generation without sensory feedback; i.e. the motor patterns released by command neurons are centrally programmed (Hughes & Wiersma, 1960; Wiersma & lkeda, 1964; Evoy & Kennedy, 1967; Larimer & Kenned.y, 1969b). Deaffer- entation in command driven ",ystems may cause changes in the motor discharge pattern, but the basic response remains. These data also suggest a genetic specification of connectivity.

In ar thropod systems, relatively few motor neurons are involved in the control of skeletal muscles. As movements and behaviors change; the motor neurons work in different combinations. Different behaviors may therefore be encoded in command elements by assuming that motor neurons are recruited in different ensembles depending upon the command and its related circuitry (Kennedy et al., 1969; Larimer & Kennedy, 1969b; Kennedy, 1971). A basic feature of the motor systems of many organisms is reciprocity between antag6nists. Numerous cases show that this basic reciprocity is preserved as well in command driven motor programs. Clear examples are seen in the abdominal positioning system of crayfish (Evoy & Kennedy, 1967) in the lobster swimmeret system (Davis & Kennedy, 1972a) and in the cardiac control system of crayfish (Field & Larimer, 1975). An inter- esting variation of this rule was observed however in the case of the motor control system for the tail appendages (uropods) of crayfish. Here the uropods are capable o f more varied movements than, for example, the abdomen and show movements in all planes. In some movements two or more muscles may be synergistic, but in others, these same muscles may be antagonistic. Certain commands were found to break the synergism and others to maintain it according to the appropriate plane of movement underway (Latimer & Kennedy, 1969b).

Commands which inhibit or suppress behavior are apparently fairly widespread in crustaceans. Cardiac inhibition by central interneurons has been observed in several instances 0hriersma & Novitski, 1942; Wilkens et al., 1974; Field & Latimer, 1975). Simi- laxly, units are described which slow or stop swimmeret activity (Wiersma & lkeda, 1964; Davis & Ken- nedy; 1972a, b, c) affect foregut mobility (Dando & Selverston, 1972) and ventilation rhythm (Wilkens et al., 1974). Each of these impinge on an oscillator driven system that is rather localized. Presumably, such interneurons~ it" ,---~ivated with proper timing and frequency, could provide a widened latitude for total

neural control. Another class of inhibitory commands is known which probably operate somewhat differ- ently from those just described. These arc the "sup- pression" commands observed in the abdominal positioning system (Evoy & Kennedy, 1967) and the "'statue" command described for axons emerging from the brain (Bowerman & Larimer, 1974a). In the former example the command seemed to suppress the ongoing activity or excitatory command by breaking reciprocity while lowering output in both antagonistic muscles. The "statue" command on the other hand was observed to freeze the entire animal, including appendages and abdominal geometry, into any position the crayfish assumed between stimulations. This response is remarkable in the sense that the effects are so widely distributed. The mechanisms underlying the two responses are not understood, but could be related. If reciprocity were broken to all the antagonistic muscles there would be some locking of joint positions, however, it is difficult to explain tile posit- ional independence of the response. Another mechanism which might contribute to freezing of position could be a generalized gating on of resistance reflex~, but this too is not totally satisfactory. It is clear, however, that there must be a mechanism other than widespread central and peripheral inhibition occurring since this would tend ~o produce a limp configuration dominated by the influence of gravity.

Only a few speculations have emerged concerning the organization of command systems largely because of their apparent complexity and the lack of direct morphologi~-al data. The lateral giant fiber system is an exception however, and as a result, a rather complete explanation of its organization and activation is known (Zucker et al., 1971 ; Zucker, 1972a, b, c). The lateral giant fibers are large interneurons that are pre- motor to many of the fast flexor motor neurons supplying the abdominal muscles (Kennedy & Takeda, 1965a: Kennedy et al., 1969: Larimer et ai., 1971). The morphology of the lateral giants has been revealed by dye injection (Remler et aL, 1968; Larimer et aL, 1971) as have many of the associated interneurons and motor neurons (Selverston & Kennedy, 1969; Otsuka et aL, I967; Selverston & Remler, 1972; Krasne & Sliding, 1972; Mittenthal & Wine, 1973). When the morphology was skilfully combined with extensive intracellular and extraceltular recording, Zucker (1972a) was able to provide a neural circuit for the lateral giant command (see also Zucker et al., 1971). Basically the lateral giants are activated by touching the abdominal pleura. Thus the circuit begins with many tactile receptors which impinge" with chemical synapses on only three large multiseg- mental tactile interneurons. The tactile interneurons (as well as a few terminals of the receptors) in turn synapse with electrical junetion~ on the lateral giant neuron and upon each other. The giants finally synapse, also with electrical junctions, on some of the fast flexor moto r neurons (Larimer et a/., 1971; Mit- tenthal & Wine, 1973). Several features of this system are of interest. First, it is a cascading one which places the lateral giant interneurons in a "decision making ~ position, albeit one of merely distributing the ir/strue- tion t o the motor neurons. There is a predominance of electrical junctions particularly on the lateral giant where a high voltage threshold must be overcome.

4 ROBERT 17. BOWfRMAN AND .lAMES L. L.ARIMER

Ahhough this overall organization could serve well as a model for dissecting other command circuits, dif- ficulties are anticipated in unraveling the more complex command systems since they typically incorpor- ate one or more neural oscillators, neural t iming and coupling systems, and mult imodal inputs for triggering as well :is widely distributed haotor outputs.

CONCLUSION

Numerous questions remain concerning the role of command elements in the generation of normal behavior (see Maynard, 1973; Kennedy & Davis, 1975). One of the most basic of these questions is whether moxements in freely behaving animals are normally driven by the selective activation of appropriate command fibers. Limited information bearing on this problem (in arthropods) was obtained by chronic recording from the CNS of crayfish during escape and swimming (Schrameck. 1970; Wine & Krasne, 1972) where impulses in the giant fibers were shown to accompany some swimming movements (Bowerman & Latimer, 1974b). Thus impulses in the small interneurons may have been responsible for some escape- like behaviors while their activity went undetected. Other evidence, although indirect, supports the underlying role of command fibers. For example, the volitional motor programs for abdominal positioning in crayfish resemble closely those evoked from various command fibers (Evoy e t a l . , 1967: Larimer eral . . 1971: see also Dorsett e ta l . , 1969). From the variety of commands now known, including complex odes (Bowerman & Latimer, 1974a, b). it is possible to account for a substantial number of the commonly seen behaviors of crayfish. Perhaps the "releasers" of classical ethology operate by gating on a behavior that is genetically fixed in the circuits of one or more Command elements (see Konishi, 197l). Unfortun- ately, we are still far from realizing such an under- standing of the roles of command interneurons.

Other questions concern ing the position of command fibers in the neural heirarchy, whether they operate alone or in groups, whether single neurons can routinely evoke different behaviors depending upon frequertey or pattern of activity, or their com- bination with others, whether more than one command can actually evoke the same behavior; i.e. is there redundancy, all remain largely unanswered, or disagreement, at least, persists (Maynard. 1973).

The modern techniques of neurobiology are being applied to these problems, and can be expected to yield answers in the near future. Even if command neurons are found to be less important than we now assume them to be, they will probably continue to receive considerable attention in the near future as we learn more about how the nervous system is organized.

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command neurons in crustaceans

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