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First published online June 29, 2006
Journal of Experimental Biology 209, 2607-2609 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02358
JEB Classics |
SMALL CUTICULAR DOMES ARE STRAIN RECEPTORS
Georg-August-Universitat
rhuster{at}gwdg.de
Proprioceptors are sense organs recording the relative position of body
parts or internal tissues. The history of proprioceptor research is often
characterized by long delays between a sensory structure's discovery and its
functional characterization. A classic example of one such delay is the
lengthy period between the anatomical indentification of vertebrate muscle
spindles by A. Kölliker (Kölliker, 1862) and W. Kühne
(Kühne, 1862) and the discovery of their proprioceptive role six decades
later (Matthews, 1928
). It was
only in the 1960s that Ake B. Vallbo and Karl-Erik Hagbarth made heroic
recordings from muscle spindle afferents in their own arm nerves (Vallbo and
Hagbarth, 1967) to demonstrate the structures' natural function as tension
receptors. In this JEB Classics article, I describe how research into the
function of the small dome-shaped sensilla found on the insect cuticle
followed a similarly lengthy but less tortured course, culminating in
Pringle's classic 1938 paper describing the function of the campaniform
sensilla (Pringle,
1938a).
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First described by J. B. Hicks in the mid nineteenth century
(Hicks, 1857) and termed
`sensilla campaniformia' in 1909 (Berlese,
1909), early speculation on their function centred around their
possible chemosensory role. However, R. Vogel also suggested that the
structures may have a mechanosensory function
(Vogel, 1911). The conundrum
was resolved in Pringle's groundbreaking paper on the maxillary palp
campaniform sensilla in cockroaches, when he clearly showed that these
intriguing structures respond to strain and are mechanosensory proprioceptors
(Pringle, 1938a). These were
the first proprioceptors to be described, both functionally and down to the
level of single, or a few, sensory cells.
This remarkable breakthrough was made possible by the development of new
electrophysiology technologies at the end of the 1920s, when physiologists
studying sensory and motor systems in animals and humans first gained access
to preamplifiers, oscilloscopes (Matthews,
1928) and audio-monitors, offering them the first opportunities to
study nerve and muscle action potentials directly. By the early 1930s, after
the publication of an increasing number of studies on vertebrate sensory and
motor systems, the young J. W. S. Pringle noted that recordings from sensory
nerves in vertebrates revealed both the characteristics of sensory signals and
the information they encoded for the central nervous system (CNS). The first
studies by Richard Julius Pumphrey of insect afferent action potentials
directed towards the CNS from external receptors, such as mechanosensory
spines and hairs (Pumphrey,
1936; Pumphrey and
Rawdon-Smith, 1937), shed light on insect exoskeleton sensory
responses and inspired Pringle's own studies.
However, Pringle's early attempts to apply these new techniques to insect
chemoreceptors proved unsuccessful. Focusing on the cockroach mouthparts
(palps), which in many insects continuously probe the chemical nature of
possible food sources, Pringle may first have tried to find responses in
ascending sensory nerves from chemoreceptors at the palps' tips. But it is
still impossible, even today, to make nerve recordings with extracellular
electrodes from the chemosensory cells' tiny axons. However, Pringle
successfully obtained reliable neural responses whenever he physically
disturbed the palps, especially when the joints between segments of the
cuticle were moved. Able to distinguish these signals from the fast adapting
responses of the palps' tactile hairs, which had been found on the insect's
legs by Pumphrey a few years earlier
(Pumphrey, 1936), Pringle made
the groundbreaking discovery that the campaniform sensilla are mechanosensors.
The results were published in 1938
(Pringle, 1938a); the paper
also included the first full account of sensory function in a specific insect
sensillum and established a new style of morphological and functional
description in neural tissue, outlining the location and innervation of a
specific sensillum type prior to analyzing the functional and
electrophysiological properties of primary afferents.
Was it luck or insight that inspired Pringle to choose campaniform sensilla on cockroach palps as his first subject? Probably a mixture of both. The palp's campaniform sensilla are associated with the hinge-like articulations between the segments of the palps. Therefore, it is clear how compression of the cuticle, either by bending, release from bending or lengthwise strain on the palp's cuticle, affects the campaniform sensilla near the joint hinges causing their oval caps to bulge or flatten, which in turn produces strain in the underlying sensory neuron to generate afferent impulses directed to the CNS. This allowed Pringle to show that campaniform sensilla are exteroreceptors, which record strain due purely to external forces. Another fortunate property of Pringle's cockroach palpus preparation was that he could monitor the campaniform sensilla's responses to forces produced by the palp's own muscles, which also allowed him to show that campaniform sensilla function as proprioceptors (receptors that record internal strain caused by resistance to muscle tension). Furthermore, Pringle's palpus preparation allowed him to focus on responses from pairs or small groups of campaniform sensilla near single joints when he cut distal segments and recorded selectively from the remaining 1-3 campaniform sensilla. By selecting responses from small groups of the mechanosensors, he could identify their slowly adapting action potential frequency responses, which he selected by a primitive method of amplitude filtering: he simply turned down the monitoring loudspeaker to hear the largest impulses alone. But from here Pringle turned to very speculative thinking: unable to distinguish the uniform amplitude impulses measured simultaneously from two or three campaniform sensilla, he assumed that sensory axons can merge and form a single afferent fiber, which has never been found.
In summary, Pringle's paper (Pringle,
1938a) on proprioception in cockroach palps was the first to
completely describe the function of single campaniform sensilla, and proved to
be the benchmark for subsequent proprioceptor studies. Since then, whenever
questions about campaniform sensilla function have been raised, the answer is
usually prefaced with `Pringle showed that'. Even Pringle's own companion
paper on the trochanteral campaniform sensilla of legs, which includes a
superb description and discussion of the campaniform sensilla's potential
kinaesthetic function [allowing the insect to detect its own movement and
position (Pringle, 1938b)],
did not match the clarity of data that he derived in the palp study. He
compensated for this in the leg study by developing a functional model of the
limb's campaniform sensilla, which demonstrated that cuticle compression
elevates the sensor's cuticular cap to stretch the attached dendrite and
initiate an impulse. But even this model could not determine which axis of the
oval-shaped campaniform sensilla provides the greatest mechanical sensitivity
by deforming the most in response to compression - a problem that haunted most
papers on campaniform sensilla until Stanley Spinola and Kent Chapman proved
that compression perpendicular to the main axis in oval domed campaniform
sensilla produces the most effective stimulation
(Spinola and Chapman,
1975).
Having acknowledged that insect campaniform sensilla behave as strain
sensitive proprioceptors, Pringle and his colleague, G. Fraenkel, were able to
interpret the proprioceptive function of groups of campaniform sensilla at the
halteres (Pringle and Fraenkel, 1938), oscillating club-shaped appendages that
have replaced the hindwing structures in flies and had long been suspected of
involvement in flight steering (Weinland,
1890). Much later, after the war, Pringle proved such a mechanism
in detail by recording from nerves in freely moving halteres and found that
specific campaniform sensilla groups associated with the oscillating halteres
record path deviation parameters during axial movements of the fly's body.
Much later this led to the detection of the most rapid neural pathway in
insects ever identified, between the electrically coupled haltere afferents
and the motoneurons of the fly's steering muscles
(Fayyazuddin and Dickinson,
1996).
Detailed work on the functions of insect campaniform sensilla continued in
the 1960s and 1970s, focussing initially on the functional morphology of
different campaniform sensilla types in various locations
(Chapman, 1965; Moran et al.,
1971). The proprioceptive and kinaesthetic roles of campaniform sensilla were
revisited even later in the 1980s from the perspective of their central neural
connections, by tracing the neural connections from single insect receptors to
the insect CNS (Hustert et al.,
1981). Further locomotor studies dealt specifically with neural
control in response to limb loading and unloading
(Zill, 1981;
Laurent and Hustert, 1988;
Ridgel et al., 1999;
Höltje and Hustert, 2003;
Akay et al., 2004). To this day
the question whether campaniform sensilla are the main source of gravitational
information for the insect CNS remains unresolved. Although most insects
appear to lack a specialized sense of gravity, campaniform sensilla are
currently believed to be the possible seat of the gravitational sense in
insects, but this has yet to be confirmed.
When Pringle initiated his study of cockroach palp campaniform sensilla in pre-war Europe, he had little idea of the legacy his paper would leave and the inspiration it would offer well into the 21st Century, making it a justifiable JEB Classic.
References
Akay, T., Haehn, S., Schmitz, J. and Büschges, A.
(2004). Signals from load sensors underlie interjoint
coordination during stepping movements of the stick insect leg. J.
Neurophysiol. 92,42
-51.
Berlese, A. (1909). Gli insetti,Vol. I, p.1004 . Milano: Società Editrice Libraria.
Chapman, K. M. (1965). Campaniform sensilla on
the tactile spines of the legs of the cockroach. J. Exp.
Biol. 42,191
-203.
Fayyazuddin, A. and Dickinson, M. H. (1996). Haltere afferents provide direct, electrotonic input to a steering motor neuron in the blowfly, Calliphora. J. Neurosci. 16,5225 -5232.
Fraenkel, G. and Pringle, J. W. S. (1938). Halteres of flies as gyroscopic organs of equilibrium. Nature 141,919 -920.
Hicks, J. B. (1857). On a new organ in insects. J. Proc. Linn. Soc. (Zool). 1, 136-140.
Höltje, M. and Hustert, R. (2003). Rapid
mechano-sensory pathways code leg impact and elicit very rapid reflexes in
insects. J. Exp. Biol.
206,2715
-2724.
Hustert, R., Pflüger, H.-J. and Bräunig, P. (1981). Distribution and specific projections of mechanoreceptors in the thorax and proximal leg joints of locusts. III. The external mechanoreceptors: The campaniform sensilla. Cell Tiss. Res. 216,97 -111.[Medline]
Koelliker, A. (1862). Untersuchungen über die letzten Endigungen der Nerven. Mit 4 Kupfertafeln. Leipzig: W. Engelmann.
Kuehne, W. (1862). Über die peripherischen Endorgane der motorischen Nerven. Mit 5 Tafeln. Leipzig: W. Engelmann.
Laurent, G. and Hustert R. (1988). Motor neuronal receptive fields delimit patterns of motor activity during locomotion of the locust. J. Neuroscience 8,4349 -4366.[Abstract]
Matthews, B. H. C. (1928). A new electrical
recording system for physiological work, J. Physiol.
65, 225.
Pringle, J. W. S. (1938a). Proprioception in insects. I. A new type of mechanical receptor from the palps of the cockroach. J. Exp. Biol. 15,101 -113.[Abstract]
Pringle, J. W. S. (1938b). Proprioception in insects. II. The action of the campaniform sensilla on the legs. J. Exp. Biol. 15,114 -131.[Abstract]
Pumphrey, R. J. (1936). Slow adaptation of a tactile receptor in the leg of the common cockroach. J. Physiol. 87,6P -7P.
Pumphrey, R. J. and Rawdon-Smith, A. F. (1937). Synaptic transmission of nervous impulses through the last abdominal ganglion of the cockroach. Proc. R. Soc. B, 1937,106 -118.
Ridgel, A. L., Frazier, S. F., DiCaprio, R. A. and Zill, S.
N. (1999). Active signaling of leg loading and unloading in
the cockroach. J. Neurophysiol.
81,1432
-1437.
Spinola, S. M. and Chapman, K. M. (1975). Proprioceptive indentation of the campaniform sensilla of cockroach legs. J. Comp. Physiol. 96,257 -272.[CrossRef]
Valbo, A. B. and Hagbarth, K. E. (1967). Impulses recorded with micro-electrodes in human muscle nerves during stimulation of mechanoreceptors and voluntary contractions. Electroenceph. Clin. Neurophysiol. 23, 392.[Medline]
Vogel, R. (1911). Über die Innervierung der Schmetterlingsflügel und über den Bau die Verbreitung der Sinnesorgane auf Denselben. Z. Wiss. Zool. 98, 68-134.
Weinland, E. (1890). Über die Schwinger (Halteren) der Dipteren. Z. Wiss. Zool. 51, 55-166.
Zill, S. N. and Moran, D. T. (1981). The exoskeleton and insect proprioception. I. Responses of tibial campaniform sensilla to external and muscle generated forces in the American cockroach, Periplaneta americana. J. Exp. Biol. 91, 1-24.
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