The angular acceleration receptor system of the statocyst of Octopus vulgaris : morphometry, ultrastructure, and neuronal and synaptic organization

Abstract

The angular acceleration receptor system (crista/cupula system) of the statocyst of Octopus vulgaris has been thoroughly reinvestigated, and detailed information is presented regarding its morphometry, ultrastructure, and neuronal and synaptic organization. In each of the nine crista sections, some receptor hair cells are primary sensory cells with an axon extending from their base. Also, there are large and small secondary sensory hair cells without axons, which make afferent synapses with large and small first-order afferent neurons. The afferent synapses are of two morphologically distinct types, having either a finger-like or a flat postsynaptic process; both can be seen in the same hair cell. In addition to the afferents, there is a dense plexus of efferent fibres in each crista section, and efferent synapses can be seen at the level of the hair cells and of the neurons. The morphometric analysis of the nine crista sections shows obvious differences between the odd-numbered (C1, C3, C5, C7, C9) and the even-numbered (C2, C4, C6, C8) crista sections: they differ in length, in the number of the small primary sensory cells and in the number of the small first-order afferent neurons. Centrifugal cobalt filling of the three crista nerves revealed a disproportionate innervation of the nine crista sections: the anterior crista nerve innervates section C1 and the first half of section C2, the medial crista nerve innervates the second half of section C2, sections C3, C4, C5, and the first half of section C6, and the posterior crista nerve innervates the second half of section C6, and sections C7, C8 and C9. In each of the three crista nerves, only 25% of the total number of axons are afferent fibres, the remaining 75 % are efferent. To each of the nine crista sections a cupula is attached. In the form and size of the cupulae there is again a conspicuous difference between the odd and the even crista sections: a small widebased cupula is attached to each of the odd crista sections, whereas the even crista sections each have a large narrow-based cupula with a small area of attachment. The results are discussed with reference to their functional consequences.

Structure and function of the Nautilus statocyst

“…In contrast, polarized hair cells are part of either gravity or angular acceleration receptor systems; the latter systems contain exclusively polarized hair cells. In Nautilus, the arrangement of kinocilia in an elongated row (type A hair cell) is similar to that found in the polarized hair cells of the statocysts of coleoid cephalopods (Octopus, Sepia and Loligo;Barber 1968;Budelmann et al 1973Budelmann et al , 1987aBudelmann 1979Budelmann , 1988, and as well in the neck receptor organ of the squid Lolliguncula and presumably of other decapods (Preuss & Budelmann 1995a). …”

“…they carry an axon. This is different from the situation in the fast moving coleoid cephalopods where the receptor epithelia are composed of, or include, secondary sensory cells (without an axon) which allow signal convergence from several receptor cells onto one first-order afferent neuron (Klein 1932;Budelmann 1976Budelmann , 1977Budelmann & Thies 1977;Colmers 1981;Budelmann et al 1987a).…”

“…In octopods, on the other hand, locomotion is slower (crawling and slow swimming) and, therefore, their statocysts are less complex. They are sphere like and have only one macula/statolith system (Young 1960); their crista/cupula system, however, has nine segments and is subdivided into two systems of different sensitivity presumably to detect angular accelerations during slow crawling as well as faster swimming (Young 1960;Williamson & Budelmann 1985a, b;Budelmann et al 1987a, b). Nautilus shows the lowest level of mobility (Chamberlain 1990) and its statocysts are the least differentiated, with no obvious gross morphological expression of an angular acceleration system such as is known in its coleoid relatives.…”

“…In fast moving coleoid cephalopods, such as octopuses, cuttlefish and squids, orientation with respect to gravity and angular accelerations is well known and their equilibrium receptor organs (statocysts) include receptor systems for the detection of gravity and angular accelerations (Young 1960;Budelmann et al 1987a;Budelmann 1990). As in vertebrates, information from these two systems is centrally integrated with visual and proprioceptive informations to optimize equilibrium control, such as during compensatory eye movements (including postrotatory nys-tagmus) and compensatory head and body movements (Budelmann 1970(Budelmann , 1990Collewijn 1970;Messenger 1970;Budelmann & Young 1984;Preuss & Budelmann 1995a).…”

Comparative & Invertebrate Neuroscience

“…Vertebrate vestibular systems have powerful, but relatively small, efferent innervations, with between 8 and 18 % of the axons in the vestibular nerve being efferent fibres (Goldberg & Fernandez, 1980). In contrast, 75% of the axons in the analogous octopus statocyst nerve are efferent fibres (Budelmann et al 1987). Acetylcholine (ACh) has been identified as a likely efferent neurotransmitter in both vertebrates (Guth et al 1986) and cephalopods (Auerbach & Budelmann, 1986) and, as part of a program to investigate the operation of the cephalopod efferent system, we have studied the action of acetylcholine on the dissociated sensory hair cells of the octopus statocyst.…”