Morphological evidence for local microcircuits in rat vestibular maculae

Abstract

Previous studies suggested that intramacular, unmyelinated segments of vestibular afferent nerve fibers and their large afferent endings (calyces) on type I hair cells branch. Many of the branches (processes) contain vesicles and are presynaptic to type II hair cells, other processes, intramacular nerve fibers, and calyces. This study used serial section transmission electron microscopy and three-dimensional reconstruction methods to document the origins and distributions of presynaptic processes of afferents in the medial part of the adult rat utricular macula. The ultrastructural research focused on presynaptic processes whose origin and termination could be observed in a single micrograph. Results showed that calyces had 1) vesiculated, spine-like processes that invaginated type I cells and 2) other, elongate processes that ended on type II cells pre- as well as postsynaptically. Intramacular, unmyelinated segments of afferent nerve fibers gave origin to branches that were presynaptic to type II cells, calyces, calyceal processes, and other nerve fibers in the macula. Synapses with type II cells occurred opposite subsynaptic cisternae (C synapses); all other synapses were asymmetric. Vesicles were pleomorphic but were differentially distributed according to process origin. Small, clear-centered vesicles, approximately 40-60 nm in diameter, predominated in processes originating from afferent nerve fibers and basal parts of calyces. Larger vesicles approximately 70-120 nm in diameter having approximately 40-80 nm electron-opaque cores were dominant in processes originating from the necks of calyces. Results are interpreted to indicate the existence of a complex system of intrinsic feedforward (postsynaptic)-feedback (presynaptic) connections in a network of direct and local microcircuits. The morphological findings support the concept that maculae dynamically preprocess linear acceleratory information before its transmission to the central nervous system.

The Role of Sensory Network Dynamics in Generating a Motor Program

“…In this extreme example, a sensory organ ceases to inform the nervous system about the environment and starts generating information independently. Less extreme situations may occur in the auditory (Wu and Oertel, 1986;Sobkowicz et al, 2003Sobkowicz et al, , 2004, vestibular (Ross, 1997;Uchino et al, 1999), visual (Dowling, 1970;Dacheux and Raviola, 1986;Wassle and Boycott, 1991;Masland and Raviola, 2000;Tsukamoto et al, 2001;Volgyi et al, 2002), and olfactory (Rall et al, 1966;Hinds, 1970;Kosaka and Hama, 1982;Kosaka et al, 2001;Laurent et al, 2001;Nezlin et al, 2003) systems in which elaborate interconnections and feedback exist. In such interconnected systems, the connectivity presumably can produce a more complex dynamics than the one necessary for the processing of the sensory signal but at the same time can be controlled by higher centers and altered, as the behavioral context requires it.…”

Ultrastructural observations of efferent terminals in the crista Ampullaris of the toadfish, opsanus tau

“…Somal spines or leaflets often interdigitate between adjacent efferent and afferent endings. As noted by other investigators using similar tissue processing techniques (Hama 1969;Chang et al 1992;Lysakowski 1996;Lysakowski and Goldberg 1997;Ross 1997), the distinction between efferent and afferent endings is usually straightforward. Profiles of afferent endings have electron-lucent cytoplasm and occasional postsynaptic densities seen in association with hair cell-afferent synaptic body synapses.…”

“…Scale bar: 2.5 µm hair cells. Although vesicle-containing afferent terminals have been reported to form reciprocal synapses with type II hair cells in other systems (Lysakowski 1996;Lysakowski and Goldberg 1997;Ross 1997), no such contacts were observed in our material. The identity of approximately 1% of the profiles was equivocal; these were excluded from consideration.…”

Reciprocal Innervation of Outer Hair Cells in a Human Infant

“…Second, there is precedence for a ®rst-order``afferent'' neuron to also form``efferent'' synapses on receptor cells in other sensory systems, such as the vestibular macula (Ross et al 1997;Chimento and Ross 1996) and the carotid body Mitchell 1975, 1981).…”

“…This type of synaptic relationship has been described in both the central and peripheral nervous systems. Reciprocal synapses are common in the brain (Famiglietti 1970;Guan et al 1995;Marcos et al 1996), retina (Harveit 1999;Dowling 1968), olfactory bulb (Kirillova and Lin 1998;Isaacson and Strowbridge 1998), autonomic nervous system (Kawai 1996;Yagamuchi et al 1975), carotid bulb (McDonald and Mitchell 1975;Matsumoto et al 1980), and vestibular macula (Ross 1997;Dunn 1980;Lysakowski and Goldberg 1997). In the organ of Corti, reciprocal synapses are characterized by the presence of both afferent and efferent types of synaptic membrane specializations between a single nerve ®ber and a hair cell (Nadol 1981).…”