© 2002 by The Society for Integrative and Comparative Biology
Modulation of the Crayfish Escape Reflex—Physiology and Neuroethology1
1 Department of Psychology, UCLA, Los Angeles, California 90095-1563
2 Department of Biology, Georgia State University, Atlanta, Georgia 30302-4010
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We review here factors that control the excitability of the giant neuron-mediated tail-flip escape behavior in crayfish, focusing especially on recent findings concerning serotonergic modulation. Serotonin can either facilitate or inhibit escape depending on concentration and pattern of application. Low concentrations facilitate while high ones inhibit; however, if high concentrations arise gradually they facilitate instead of inhibiting. The effects of serotonin can also be altered by social experience, with application regimens that cause facilitation in social isolates coming to produce inhibition after an extended period of living as a subordinate. Attempts to understand both the possible physiological basis of some of these complexities and their possible function are discussed. Neuroethological investigations indicate that giant neuron-mediated escape is inhibited during the initial fights that establish social relationships and is facilitated in their immediate aftermath. Once the relationship of a pair is well-established, the presence of the dominant tends to suppress giant neuron-mediated escape (but not tail-flip escape mediated by non-giant circuitry) in the subordinate, but the presence of the subordinate has relatively little effect on the dominant. These patterns of modulation can be seen as consistent with the known variations in serotonin's effect as a function of concentration and social experience and may provide a biological reason for these variations.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONTHE NEURAL CIRCUITRY UNDERLYING...MODULATION AND PLASTICITY IN...NEUROETHOLOGY OF GF MODULATION...References |
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For most neurobiologists it is an article of faith that the behavior which emerges from nervous systems is the product of a neural machine. But the machine is one in which a given neural circuit does not always work the same way. Operational properties of a circuit can change due to learning and due to modulation by other circuits, imparting to the behavior of a given individual the great variety and irregularity that makes the behavior of animals and ourselves interesting and a challenge to our understanding. To a great degree, though not entirely, changes in the properties of neural circuits are due to changes in the functional properties of their synapses.
The last several decades have seen remarkable progress in uncovering various forms of synaptic plasticity induced either by activity or by chemical modulators. Some of the first forms of synaptic plasticity to be described and related to behavioral plasticity were in invertebrates—specifically in Aplysia (see articles by Sutton and Carew, 2002, and Sherff and Carew, 2002 [this issue]; Kandel, 1976
) and also in crayfish (Krasne, 1969; Zucker, 1972; Zucker et al., 1971). In parallel with these studies on invertebrates were discoveries beginning at roughly the same time on mammalian hippocampal LTP (Bliss and Collingridge, 1993), which is now widely regarded as a possible mechanism of associative learning. This latter line of work has led to a veritable frenzy of activity directed both at working out cellular and molecular mechanisms of long-term potentiation (LTP) and at trying to fathom what might be its actual roles visa vi behavior. Research on LTP has somewhat eclipsed invertebrate research, but invertebrate systems continue to provide unique opportunities: (1) The connection between cellular phenomena and behavior is often much clearer in invertebrates due to the relative simplicity of some of their behavior-producing neural circuitry; thus, we can discover the natural uses made of instances of plasticity and modulation. (2) The very diversity of invertebrates inevitably exposes us to a wider array of phenomena than we would see from studying mammals alone; thus it helps us distinguish what is general from what is not.
We review here work on plasticity seen in the neural circuitry which mediates escape behavior in crayfish, with a focus on recent surprising findings on serotonergic modulation, and their possible functional significance.
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THE NEURAL CIRCUITRY UNDERLYING ESCAPE BEHAVIOR |
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Escape can be mediated in two rather different ways as indicated separately on the left and right of Figure 1A (for a review see Edwards et al., 1999
). The circuitry on the left produces either of two distinct types of response, depending on locus of stimulation. Each response type is associated with a giant command neuron. The medial giants (MGs) sum input from anterior sensory channels and make output connections with giant flexor motor neurons (motor "giants"—MoGs in Fig. 1) that cause a dart backwards when the excitation produces even one spike in the MGs. The lateral giants (LGs) sum input from posterior channels and cause an upward rotation that distances the hind end of the animal from the disturbing stimulus. MG and LG responses are often referred to as "reflex" responses or as "giant fiber (GF)" responses for the giant axons of the MGs and LGs, which run the length of the nerve cord. GF responses are very prompt (muscle potentials can begin within 3 msec) and are good at getting the crayfish moving away from the source of stimulation rapidly.
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The circuitry on the right has no giant neurons (non-G circuitry), is much more complex, and is far from fully charted. Whereas the giant-containing circuitry produces only two very stereotyped forms of response ("back" and "upward rotation") and always single flexions, the responses generated by the non-giant circuitry have a seemingly infinite variety of possible forms and can occur in repetitive strings ("swims"). Using this circuitry crayfish can move directly away from an oblique stimulus, avoid obstacles, and move toward specific locations. Unlike GF responses, which ordinarily occur only in response to abrupt and fairly vigorous stimulation, non-G responses are often prompted by gradually developing threats. The more sophisticated responses of the non-G circuitry come at a price: They are far from prompt (latencies are about 100 msec).
Before beginning to discuss forms of synaptic modulation that have been studied in the GF circuitry it should be noted that only the synapses between primary afferents and the sensory interneurons of the GF circuitry are conventional chemical synapses. The remainder are voltage-gated electrical synapses, which pass current effectively only when the presynaptic side of the synapse is made positive relative to the postsynaptic side by the arrival of a presynaptic spike (Edwards et al., 1991; Furshpan and Potter, 1959; Giaume et al., 1987; Jaslove and Brink, 1986). Qualitatively, these voltage-gated electrical synapses have many of the same properties as chemical synapses. These include polarized transmission, temperature sensitive synaptic delay, and modulation of EPSP size by postsynaptic membrane potential level. Because of these similarities it can be very difficult to distinguish voltage-gated electrical synapses from chemical ones, and as we shall see, EPSPs produced by these electrical synapses are also subject to modulation of kinds that one normally associates with chemical synapses.
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MODULATION AND PLASTICITY IN GF CIRCUIT |
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The first form of plasticity discovered in GF circuitry circuit was intrinsic depression of transmitter release as the result of repetitive presynaptic activity at the cholinergic synapses made onto sensory interneurons that innervate the LGs (Fig. 2, line 1; Krasne, 1976
; Miller et al., 1992; Zucker, 1972). Like probably all escape behavior, GF responses habituate to repeated stimulation, and this presynaptic activity-dependent depression is at least in part responsible. Its discovery in the late 60s was exciting, because it was one of the first times that a simple kind of learning had been traced to a specific neural mechanism.
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It was soon after found that a second influence affecting whether crayfish will escape to threats is a GABA-ergic inhibitory input directly to the GF dendrites (Fig. 2, line 2; Krasne and Wine, 1975
; Vu and Krasne, 1993; Vu et al., 1993). This inhibition, which is controlled by higher centers, is turned on under a variety of circumstances and greatly elevates the stimulus threshold for producing GF escape. This "tonic inhibition" contributes to habituation (Krasne and Teshiba, 1995) and also serves to elevate GF escape thresholds when, for example an animal has found a food source and is avidly feeding (Krasne and Lee, 1988) or when an animal is firmly clutched by a fisherman and reflex tailflips would be useless (Krasne and Wine, 1975).
Recently, work done by former students from each of our laboratories has begun to suggest that transmission at the voltage-gated electrical synapses on the GFs is also subject to intrinsic, activity-dependent change. In both their experiments, as in other experiments to be discussed here, brief electrical test shocks to sensory nerves were delivered every few minutes and responses recorded in the LGs with intracellular microelectrodes. The shocks produce compound excitatory postsynaptic potentials (EPSPs) (Fig. 1B), which have a first elevation (the 
component) resulting from monosynaptic input from the primary afferents and a second (the ß component), which is due to input arriving via the sensory interneurons. Shi-Rung Yeh (personal communication) has found that several second long trains of 4 Hz stimuli to the afferents cause both the monosynaptic and disynaptic components of LG EPSPs to grow and stay high for many hours (Fig. 3, top; Fig. 2, line 3). The augmentation is specific to input pathways that were given the 4 Hz stimulation and seems to be entirely prevented if the calcium ion chelators BAPTA or EGTA were previously injected into the LGs. Thus, this phenomenon is similar to LTP at glutamatergic synapses in that its induction is dependent on a transient elevation of calcium ions in the postsynaptic neuron. Since these are voltage-dependent electrical synapses and not glutamatergic ones, this is an interesting parallelism. Sun Hee Lee has found that similar stimulation (5 Hz) given for the much longer time of 5 min causes a depression that also lasts a long time and is blocked by BAPTA in the LGs (Lee, 1996; Lee and Park, 1997). This long-term depression (LTD)-Iike phenomenon seems to occur mainly in the disynaptic (ß) EPSP but presumably still involves depression at synapses directly on the LGs, since it is blocked by preventing calcium ion elevation in the LGs. The functional consequences of LTP are quite unknown, but it seems possible that the LTD may play some role in habituation (Fig. 2, line 4).
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Aminergic neuromodulation of transmission to the LGs
The story that is the major focus of this review began about 20 yr ago when Ed Kavitz and his students (Livingstone et al., 1980
; Kravitz, 1988) discovered that injection of serotonin into lobster or crayfish altered synaptic transmission at certain neuromuscular synapses and caused animals to adopt a posture that was seen as similar to that adopted by socially dominant animals, whereas octopamine, the arthropod analog of adrenaline, caused a subordinate-like posture. It seemed likely that since these agents affected postures associated with fight and flight, they might also affect escape. In particular, it was conjectured that octopamine might facilitate GF escape while serotonin might suppress it. This conjecture was soon verified. Octopamine enhances transmission at the first synapse (Fig. 2, line 5; Bustamante and Krasne, 1991; Glanzman and Krasne, 1983), and serotonin was initially found to inhibit transmission (but see further below), at least in part by an action at the level of the LGs (Fig. 2, line 6; Glanzman and Krasne, 1983; Vu and Krasne, 1993). It was found soon thereafter that traumatic stimulation also causes a facilitation of transmission at the first synapse that leads to behavioral sensitization of GF escape (Krasne and Glanzman, 1986); the possibility that this is mediated by octopamine is obvious, but it has not been established. Limited evidence also suggests that serotonin might under some circumstances share with GABA a role in the tonic inhibition mentioned above (Glanzman and Krasne, 1986, but see Vu and Krasne, 1993).
Serotonergic modulation
Though the discovery of serotonergic inhibition was consistent with the conjectures that had prompted the first test of serotonin's effects, it has recently become clear that these effects are much more complex than originally believed. Experiments done in the Edwards lab by Shi-Rung Yeh, over a decade after the first experiments showing an inhibitory effect, consistently found serotonin to have a facilitatory effect on transmission to the LGs (Yeh et al., 1996, 1997). After a period of some confusion it eventually became clear that the difference lay in the regimen of serotonin application (Teshiba et al., 2001). When serotonin is introduced as rapidly as possible (FAST in Fig. 4) and left in place for only 10–15 min (SHORT in Fig. 4), as was done in the original experiments, inhibition develops over 5–10 min and washes out at the same rate (Fig. 4, solid triangles). However, when serotonin levels are allowed to increase only gradually (SLOW in Fig. 4), reaching full concentration over some 20–30 min, and are allowed to remain in place for 30–45 min (Fig. 4, solid circles), facilitation rather than inhibition is seen, and this facilitation persists for as much as 5 hr or more even during washout (Yeh et al., 1997). The persistence of facilitation during wash requires exposures of longer than 10 to 15 min; the longevity of serotonin-induced facilitation in Aplysia is also well known to depend on duration of exposure (see Sutton and Carew, 2002 and Sherff and Carw, 2002 [this issue]). One gets persistent facilitation even with fast application if one uses a low dose of 5-HT (i.e., 10–8–10–6 M as opposed to 10–4 and above—Fig. 4, open circles).
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It is not yet known whether sertotonin alters the properties of the electrical junctions on the LGs. However, one can in part understand these modulations as reflections of altered ionic conductances in the LGs. The inhibition is associated with an increased conductance and small depolarization postsynaptically (Vu and Krasne, 1993
), which given that the equilibrium potential for chloride is about 8 mV above the resting level, is probably due to increased chloride conductance. The facilitation that is caused at low 5-HT concentrations (Fig. 2, line 7) is associated with a decreased conductance and also a depolarization (Yeh et al., 1997), which seems most likely to be due to a decreased potassium ion conductance. Thus inhibition and facilitation are due to non-mutually exclusive causes that could co-exist. Another way in which the facilitation and inhibition are independent is that that their underlying intracellular progenitors can apparently co-exist. Thus, the precursors of the facilitation appear to develop even at high doses that cause inhibition; however the inhibition prevents or masks expression of the facilitation. This can be seen when one washes out a high dose of serotonin that has been in place long enough for persistent facilitation to develop. Inhibition is seen for as long as the 5-HT is present, but when it is washed away, the inhibition gives way to facilitation (Fig. 4, open triangles, FAST, LONG, HIGH).
Although the signaling molecules that mediate 5-HT's effects in the LGs are not yet known, Figure 5 proposes the logic of an intracellular signaling scheme that could account for the complex effects of 5-HT exposure regimen on modulatory effect (see Teshiba et al., 2001). A pathway with a low 5-HT threshold and relatively slow onset produces facilitation, while a pathway with a high 5-HT threshold and faster onset produces inhibition. The buildup of the final stage signaling molecule of each pathway suppresses the formation of buildup of the final stage molecule of the other pathway. In this scheme FAST-LOW exposures cause facilitation because only the facilitatory pathway gets activated. FAST-HIGH exposures cause inhibition because signaling molecule I builds up first and prevents formation of F2; however F1 still builds despite the manifest inhibition, and when 5-HT is washed out, persisting F1 is allowed to promote the formation of F2, so facilitation then develops. With SLOW-HIGH exposures F2 builds up before 5-HT concentration reaches a level that can activate the inhibitory pathway, and F2 has reached a level where it can suppress the formation of I by the time serotonin is concentrated enough to exceed the threshold of the inhibitory pathway. These ideas have been developed into a computational model that correctly predicts (qualitatively) all of the types of modulation observed (Teshiba et al., 2001).
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The various delivery regimens used in our experiments may correspond to different modes of serotonin delivery that occur naturally. Serotonin is released both synaptically within abdominal ganglia neuropile, which could provide natural FAST, HIGH exposures and is also released into the blood as a hormone from a variety of sites, presumably providing a SLOW, LOW form of delivery (Beltz and Kravitz, 1983
; Yen et al., 1997).
Social dependence of 5-HT effects
There is yet another, and rather extraordinary layer of complexity to this story. Crayfish have long been known to form social hierarchies (Bovbjerg, 1953; Lowe, 1956). When two crayfish are brought together, one generally becomes dominant and the other subordinate after a short period of interaction (see below). Quite remarkably, social experience alters the effects of serotonin on transmission to the LGs: Whereas in social isolates low concentrations of serotonin facilitate transmission to the LGs (as discussed above), after a crayfish has lived for 1–2 wk as a subordinate, serotonin comes to inhibit transmission to the LGs (Fig. 6; Yeh et al., 1996, 1997). This is not the depolarizing, chloride conductance-increasing type of inhibition produced by high 5-HT, but a hyperpolarizing, presumably potassium conductance-increasing inhibition. Thus, whereas in isolates low concentrations of 5-HT decrease potassium ion conductance, in subordinates serotonin increases potassium ion conductance—a directly opposite effect (Fig. 2, line 8). Living as a dominant causes a more subtle change: Whereas in isolates prolonged exposure to serotonin causes facilitation that persists after washout of serotonin, dominants do not show this persistence of facilitation.
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Preliminary pharmacological experiments suggest that exposure to a vertebrate 5-HT2 receptor agonist [
-methyl 5-HT] mimics the faciltatory effects of serotonin, while a 5-HT1 agonist [1-(3-chlorophenyl) piperazine] has little effect in isolates but has a large inhibitory effect in subordinates (Fig. 7; Yeh et al., 1997). This interesting observation suggests the possibility that the transformation of serotonin's net effect from facilitatory to inhibitory might be due to the insertion of a species of 5-HT1 receptor into LG membrane or to some alteration in such a receptor's downstream signaling effects. However, the effects of the agonists in dominants belie this straight-forward interpretation, since 5-HT1 agonists also produce an inhibitory effect in dominants, while 5-HT2 agonist effects are not altered. The cloning of crayfish 5-HT receptors is in progress, and soon receptor antibodies will be used to look for changes in the amount of specific receptor types on the LGs as the result of social experience (Spitzer et al., 2001).
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These are fascinating observations. The finding that experience can alter the qualitative effect of a neuromodulator seems both new and remarkable. Moreover, when one considers that mental illnesses often seem to involve abnormalities in neuromodulation and that mental illness seems to have important experiential determinants, these observations provide a possible model for why life experiences might be so important. Especially interesting from this point of view is the observation that serotonin's effect in a subordinate can again take on the typical isolate profile if the subordinate is re-isolated, or can take on the profile typical of a dominant if the subordinate is paired with an animal over which it becomes dominant. However, once an animal has been dominant long enough for its response to serotonin to take on the typical dominant profile, this profile is retained even if the animal later becomes subordinate (Yeh et al., 1997
). Thus, some experience-caused changes in neuromodulation are readily reversible, but others are not. We now have a rather long list of ways in which the GF circuitry is modifiable, and we have some plausible connections to behavior (Fig. 2). It is interesting to note that each known form of behavioral control may be due to a multiplicity of modulatory mechanisms. Thus, the roles played by each and the possibility of their interaction becomes an interesting topic for future investigation. That there are interactions seems clear. For example, if GABA is infused along with 5-HT, the persistent effects of 5-HT usually produced by prolonged application do not develop (Ghiuseli and Krasne, unpublished). And experiments in progress seem to show that in the presence of picrotoxin, which blocks the chloride channel normally opened by GABA, LTD may not be produced (Lee, Shirinyan, and Krasne, unpublished). This raises interesting questions for the future.
We turn next to the role of serotonergic modulation in the natural economy of the crayfish. It seems plausible to assume that serotonergic modulation of escape reflexes plays an important role during social interactions, since otherwise its change of effect as a function of social status makes little sense. This belief is supported by serotonin's promotion of a dominant stance (Livingstone et al., 1980) and by the more recent finding that injection of serotonin reduces the extent to which animals will retreat during fights (Huber et al., 1997). However, the general notion that serotonergic modulation of the GFs might be used during social interactions does not help to explain either the reason for the complex mix of facilitatory and inhibitory effects as a function of application regimen nor does it provide any obvious reason for the changes in serotonin's effect as a function of social status. Indeed, if one assumes that serotonin is released during agonistic encounters, one is faced with the conundrum that serotonergic modulation should make subordinates less likely to escape during social interactions than are dominants!! Obviously some information on whether and how escape is in fact modulated during social interactions would help.
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NEUROETHOLOGY OF GF MODULATION DURING SOCIAL INTERACTIONS |
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When a pair of crayfish previously unknown to each other is placed in the same living space, three phases of interaction ensue (Herberholz et al., 2001
; Issa et al., 1999): - I. The animals engage in a fight during which one animal often grasps the other and engages in "offensive" tailflips that appear to be demonstrations of dominance and strength; in lobsters seemingly similar behavior can result in the target animal's dismemberment (Huber and Kravitz, 1995). After a few minutes phase I ends and phase II is ushered in when the animal that is getting the worst of it gives up and flips away.
- II. The new dominant frequently harasses the new subordinate, which backs or flips away.
- III. After some days the relationship becomes firmly established. The subordinate cowers at the margin of the living space and appears to try to keep as low a profile as possible, resting close as possible to the substrate, while the dominant moves about freely, maintains a tall posture, and very occasionally harasses the subordinate, which slinks or flips away. The transition to phase III is illustrated in Figure 8 (Issa et al., 1999
), which shows that encounters greatly decrease over days and that retreats replace escape as the most common subordinate evasion response.
- II. The new dominant frequently harasses the new subordinate, which backs or flips away.
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Edwards' group recently developed a noninvasive procedure to record tailflips from freely behaving animals during their initial encounter in a 30 min session (Herberholz et al., 2001
). They found (Fig. 9) that during phase I there were almost no GF-mediated flips; the frequent offensive tail flips are mediated by non-giant circuitry. Since the animals are fighting vigorously and providing many of the sorts of stimuli that would ordinarily evoke GF escape, the lack of responses suggests that GF escape is inhibited. Subsequently, during phase II, the dominant harasses the subordinate a great deal and the subordinate commonly escapes either with GF or non-G responses. It appears that during this period GF excitability is elevated in both subordinates and dominants, since both animals typically make a few GF escape responses per observation period that do not appear to be caused by the sorts of sudden stimuli that are ordinarily needed to trigger GF escape. Additional GF responses are made during this period when the dominant attacks the subordinate or when the subordinate bumps into the dominant while executing a non-G escape response.
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Animals that have had considerable experience with one another (phase III) have been studied with chronically implanted stimulating and recording electrodes that could be used to directly test the excitability of the LG (Figure 10; Krasne et al., 1997
). When the sensory excitability of the animals tested apart and together was compared, it was found that, while the animals are together, the sensory threshold of subordinates is about triple its value when they are apart; in contrast, the threshold of the dominant is elevated just slightly while the animals are together.
It may seem odd that the subordinates should inhibit GF escape in the presence of their dominant partner. However, inhibition of GF escape does not mean inhibition of all escape. Subordinates do in fact execute escape responses when harassed by the dominant; however, these are virtually always non-G rather than GF responses (Krasne et al., 1997). Our interpretation of the suppression of GF responses by subordinates depends on the differing capacities of the giant and non-giant circuitry. GF responses are useful for a surprise attack when an animal is taken unawares, but the more sophisticated non-G responses are more adaptive if an animal has a chance to see its attacker coming and time to prepare. GF and non-G escape are in-effect incompatible strategies. An animal that is watching a possible attacker approach and is preparing to execute an optimal non-G response at an optimal moment should avoid the production of a stereotyped GF tail-flip, and crayfish do generally inhibit GF escape circuitry when preparing to make a non-G responses (Krasne and Wine, 1975, 1984). We suggest that subordinates are in a continual state of vigilance and that the dominant probably never takes them by surprise. If so, it is probably adaptive for subordinates to suppress GF-mediated responding. It might also make sense for excitability of non-G responses to increase in subordinates when animals are together, but this has not been tested.
These neuroethological observations are summarized at the top of Figure 11. GF escape appears to be inhibited during phase I, facilitated during phase II, and inhibited in subordinates during phase III.
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It has not yet been possible to measure serotonin levels in freely behaving animals. However, if we think of serotonin as being released when animals are engaged in an agonistic encounter, we might conjecture that serotonin levels would be high in both individuals during the contest phase and would be reduced substantially but not to zero during the early post-resolution phase. Once the relationship is firmly established, dominants seem to go about their business while largely ignoring the subordinate; thus we might conjecture that they are not then releasing serotonin. In contrast, the subordinates, which must continually be on guard against harassment by the dominant, might be expected to have a steady low level of release. This conjectured pattern is portrayed at the bottom of Figure. 11. The middle row of Figure 11 shows the modulatory effects these conjectured levels of 5-HT might produce given what we know about the effects of 5-HT on EPSPs in the LGs. During the contest phase when serotonin is high, we might expect chloride conductance-increase inhibition to operate. During the post-resolution phase, when 5-HT levels are non-zero but low and the animals response to serotonin has not yet been transformed from its isolated state, we might expect GF escape to be hyperexcitable in both members of a pair. During Phase III we would expect little modulation in the dominant under the assumption that serotonin release is negligible, whereas the conjectured low-level of 5-HT release in the subordinate should cause potassium conductance-increase based inhibition, since the response to 5-HT has had time to become transformed. Thus, the pattern of modulation of GF escape that rather plausibly might be conjectured based on what is known of serotonin's effects on the LGs matches fairly well the observed pattern of GF excitability. Of course it seems likely that modulation by GABA-ergic tonic inhibition also contributes to the observed modulations of excitability. Nevertheless we can now see possible functional correlates of the complex serotonergic modulatory phenomena that physiological studies have uncovered.
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1 From the Symposium Recent Advances in Neurobiology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: krasne{at}psych.ucla.edu
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References |
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