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First published online February 27, 2009
Journal of Experimental Biology 212, 749-751 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.021972
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JEB Classics |
EXCITATION AND HABITUATION OF CRAYFISH ESCAPE
Georgia State University
biodhe{at}langate.gsu.edu
This paper describes one of the first attempts to analyze the synaptic basis for the release of an animal's fixed action pattern, which controls a behavior such as the crayfish escape response. It is also one of the early demonstrations that the neural mechanisms of a simple form of learning, known as habituation, are located in the central synapses of the neural circuit that produced the behavior.
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) and synaptic transmission
(Katz and Miledi, 1967). In
fish, studies on the Mauthner cell and its eight nerve inputs led to the
discovery of ephaptic inhibition, in which a positive extracellular potential
created around the axon hillock effectively hyperpolarizes the local cell
membrane and so decreases its excitability
(Furukawa and Furshpan, 1963).
In the crayfish, the story began with Wiersma's identification of the lateral
giant interneuron as key to triggering the tail flip escape in response to a
sharp tap on the animal's abdomen
(Wiersma, 1947;
Wiersma, 1938), and was
followed in a few years by the description of both rectifying electrical
synapses and depolarizing inhibition at the synapse between the lateral giant
interneuron and the giant motoneuron
(Furshpan and Potter, 1959;
Furshpan and Potter, 1957).
In each of these animals, a single spike in the giant neuron was found to
be sufficient to evoke the entire escape behavior, or fixed action pattern.
These discoveries provided strong support for the hierarchical decision
architecture proposed by Nikolaas Tinbergen
(Tinbergen, 1951), and helped
promote the notion of the `command neuron', first articulated for the circuit
that controlled swimmeret beating in crayfish
(Wiersma and Ikeda, 1964). The
lateral giant interneuron and the medial giant interneuron appeared to fit
this notion, as each excited overlapping but distinct sets of motoneurons with
a single spike to produce, respectively, an upward and a rearward escape
response (Mittenthal and Wine,
1973; Wine and Krasne,
1972).
Just as the lateral giant interneuron-mediated escape appeared to provide a
system in which the neural control of fixed action patterns could be studied,
it also appeared to provide a system where questions about the neural bases of
behavioral habituation could be asked. At the time of Krasne's paper
(Krasne, 1969), it was unclear
whether learning was mediated by intrinsic changes to the neural circuits that
controlled specific behavior patterns, as suggested by Donald Hebb
(Hebb, 1949), or whether, as in
the still new digital computers, learning resided in special circuits that
could interact with circuits controlling behavior
(von Neumann, 1958). For
crayfish escape, the relevant question was whether habituation of the escape
response occurred because the afferent pathway to the lateral giant
interneuron, or the lateral giant interneuron itself, became less excitable
with repeated stimulation, or because increasingly strong inhibition was
imposed on the lateral giant interneuron circuit from elsewhere in the nervous
system. Both possibilities were attractive. The first agreed with the then
popular view that synapses were the likely site of plasticity, whereas the
second was suggested by the fact that strongly habituated responses could be
dishabituated by a sensory stimulus that had no direct effect on escape
behavior.
Franklin Krasne approached these two questions in the same simple, direct
manner (Krasne, 1969). He used
a microelectrode to penetrate the initial segment of the lateral giant
interneuron axon where postsynaptic potentials could be recorded in response
to shock of nerves containing sensory axons that innervate the periphery. A
single, brief shock evoked a fast-rising excitatory postsynaptic potential in
the lateral giant interneuron that consisted of several depolarizing waves
whose amplitude and latency varied directly and inversely, respectively, with
the strength of the shock. The first of these waves, labeled `alpha' occurred
with such a short latency that it seemed likely to result from a direct, or
monosynaptic, input from the primary afferent axons stimulated by the shock.
The later waves, particularly the second or `beta' wave, also increased with
the stimulus shock, but often to a greater degree than the alpha wave. This
suggested that if the alpha excitatory postsynaptic potential was
monosynaptic, the beta excitatory postsynaptic potential was produced through
a pathway that was di- or tri-synaptic, involving as yet unidentified
interneurons that were likely excited by some of the same primary afferents
responsible for the alpha excitatory postsynaptic potential. Moreover, the
individual contributions of some of these interneurons to the beta excitatory
postsynaptic potential were identifiable when the excitatory postsynaptic
potential experienced a step-like variation in amplitude between stimuli as
the shock was slightly increased or decreased. Finally, the alpha excitatory
postsynaptic potential was always subthreshold for firing the lateral giant
interneuron, whereas the beta excitatory postsynaptic potential, riding on the
declining phase of the alpha excitatory postsynaptic potential, could reach
the lateral giant interneuron firing threshold with a sufficiently strong
stimulus.
These results led Krasne to conclude that (i) many primary afferents converged on the lateral giant interneuron, each to create only a small excitatory postsynaptic potential, such that even when they were synchronously active they could not excite the lateral giant interneuron; (ii) many of the same afferents also excited a set of mechanosensory interneurons that also converged on the lateral giant interneuron. These created larger excitatory postsynaptic potentials which, when summated by synchronous excitation, could excite the lateral giant interneuron.
The second experiment was the same as the first, except that the stimulus was repeated at a constant interval. If an individual stimulus was superthreshold, the first few stimuli of a series would each excite the lateral giant interneuron, but later stimuli would not. Because each lateral giant interneuron spike would trigger an escape tail flip in a freely behaving animal, these responses were the neural correlates of a behavioral habituation of the tail flip escape response to repetitive stimulation.
Once the lateral giant interneuron no longer fired, the beta excitatory postsynaptic potentials that had triggered the lateral giant interneuron spike became apparent. These excitatory postsynaptic potentials continued to fall in amplitude with repeated stimulation until they reached a plateau level of response that was characteristic of the stimulus frequency. The response declined as the different components of the beta postsynaptic potential first increased their response latency and then failed altogether, suggesting that the presynaptic interneuronal spikes would follow the same dynamic.
The beta excitatory postsynaptic potential displayed two other characteristics of behavioral habituation: their amplitude would recover, along an exponential time course, with rest (i.e. no stimulation), and their amplitude would increase with an increase in stimulus intensity, but then decline to near the earlier habituated level. These experience-dependent changes of the beta excitatory postsynaptic potential were in contrast to the alpha excitatory postsynaptic potential, which experienced none of them, and retained an amplitude proportional to the stimulus intensity.
From these results, it was clear that changes in the afferent path to the lateral giant interneuron produced a decrease in the beta excitatory postsynaptic potential of the lateral giant interneuron in response to repetitive stimulation. Moreover, because the alpha excitatory postsynaptic potentials were unaffected, these changes appeared to be confined to the response of the interneurons in the afferent path that were presynaptic to the lateral giant interneuron, or to their synaptic contacts with the lateral giant interneuron. Experiments published elsewhere showed that these changes still occurred even when synaptic inhibition, which might have caused the changes in transmission, was blocked. However, these results did not appear to account for all habituation of the escape response, which was evident behaviorally at slow stimulus repetition rates where no effect on the beta excitatory postsynaptic potential was seen in the reduced preparations that Krasne was studying.
With two simple experiments, Krasne's paper reached two major conclusions.
First, it completed the general outline for the afferent path to the lateral
giant interneuron, and therefore for the entire escape circuit. This was one
of the first, if not the first, polysynaptic circuits for a fixed action
pattern that had been so described. Second, it demonstrated that much, but not
all, of behavioral habituation of the escape response could be accounted for
by synaptic depression within one limb of the afferent path that carries
nervous signals to the lateral giant interneuron. As the paper suggested,
descending inhibition has since been shown to be the other major contributor
to habituation of the escape response when descending pathways from higher
parts of the nervous system are intact
(Shirinyan et al., 2006).
Krasne's description of both the afferent path to the lateral giant
interneuron and the role and site of synaptic depression was sustained by
Zucker's elegant study shortly thereafter, which identified the interneurons
that produce the beta excitatory postsynaptic potential and showed that
depression at synapses between the primary afferents and those interneurons
accounts for habituation of the lateral giant interneuron's response
(Zucker, 1972;
Zucker et al., 1971).
Moreover, Krasne's paper provided the foundation for many more papers that
described a host of phenomena, including protection against reafference
through presynaptic inhibition (Bryan and
Krasne, 1977; Kennedy et al.,
1974), mechanisms of serotonergic modulation
(Antonsen and Edwards, 2007;
Lee et al., 2008), and even
long-term synaptic potentiation, a process linked in other animals to
mechanisms of learning and memory (Tsai et
al., 2005).
Footnotes
Donald Edwards discusses Franklin B. Krasne's 1969 paper entitled: Excitation and habituation of the crayfish escape reflex: the depolarizing response in lateral giant fibres of the isolated abdomen.
A copy of the paper can be obtained from http://jeb.biologists.org/cgi/content/abstract/50/1/29
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