Introduction neurons that imply a convergence of multiple canal

Brain Research 880 2000 70–83 www.elsevier.com locate bres Research report Spatial distribution of semicircular canal nerve evoked monosynaptic response components in frog vestibular nuclei Hans Straka , Stefan Biesdorf, Norbert Dieringer Physiologisches Institut , Pettenkoferstrasse 12, 80336 Munich, Germany Accepted 25 July 2000 Abstract Most second-order vestibular neurons receive a canal-specific monosynaptic excitation, although the central projections of semicircular canal afferents overlap extensively. This remarkable canal specificity prompted us to study the spatial organization of evoked field potentials following selective stimulation of individual canal nerves. Electrically evoked responses in the vestibular nuclei were mapped systematically in vitro. Constructed activation maps were superimposed on a cytoarchitectonically defined anatomical map. The spatial activation maps for pre- and postsynaptic response components evoked by stimulation of a given canal nerve were similar. Activation maps for monosynaptic inputs from different canals tended to show a differential distribution of their peak amplitudes, although the overlap was considerable. Anterior vertical canal signals peaked in the superior vestibular nucleus, posterior vertical canal signals peaked in the descending and in the dorsal part of the lateral vestibular nucleus, whereas horizontal canal signals peaked in the descending and in the ventral part of the lateral vestibular nucleus. A similar, differential but overlapping, spatial organization of the canal inputs was described also for other vertebrates, suggesting a crude but rather conservative topographical organization of semicircular canal nerve projections within the vestibular nuclei. Differences in the precision of topological representations between vestibular and other sensory modalities are discussed.  2000 Elsevier Science B.V. All rights reserved. Theme : Motor systems and sensorimotor integration Topic : Vestibular system Keywords : Field potential; Topographical mapping; Vestibular nerve afferent fiber; Organotopic organization

1. Introduction neurons that imply a convergence of multiple canal

[3,4,6,10,14] or canal-otolith inputs [1,5]. At variance with The projection areas of afferent fibers from individual these reports, however, intracellular studies employing labyrinthine organs in the ipsilateral vestibular nuclei selective electrical stimulation of individual semicircular overlap to a large extent in non-mammalian [8,17,24– canal nerves demonstrated that monosynaptic responses of 26,30,37] as well as in mammalian species [11,31,32]. 28VN are typically evoked from only one of the ipsilateral Each of the vestibular nuclei receives inputs from most semicircular canal nerves cat [19,29], pigeon [42], frog labyrinthine sense organs, but the density of the innerva- [34]. Therefore, 28VN select among the available afferent tion from different vestibular sense organs varies between canal inputs and the convergence of multiple canal signals different regions. A considerable convergence of inputs onto 28VN might be mediated oligosynaptically. from different sense organs onto second-order vestibular The absence of a clear topographic order in the ana- neurons 28VN might be expected from these overlapping tomical projection zones of afferent fibers from different projection areas. In fact, a number of single unit studies semicircular canal nerves, however, does not imply the employing natural stimuli have reported best response absence of such an order at the synaptic or at the somatic orientation vectors of second- or higher-order vestibular level. The density of synaptic contacts between afferent fibers and 28VN for instance could exhibit regional differ- ences such that zones with high synaptic densities from Corresponding author. Fax: 149-89-5996-216. E-mail address : strakawifomail.med.uni-muenchen.de H. Straka. one semicircular canal nerve alternate with similar zones 0006-8993 00 – see front matter  2000 Elsevier Science B.V. All rights reserved. P I I : S 0 0 0 6 - 8 9 9 3 0 0 0 2 7 6 8 - 2 H . Straka et al. Brain Research 880 2000 70 –83 71 from other semicircular canal nerves. Since the dendrites the sylgard floor. The temperature of the bath was elec- of 28VN are long and select their appropriate semicircular tronically controlled and maintained at 1460.28C. canal input it is also conceivable that the cell bodies of 28 For electrical stimulation of individual semicircular canal nerves with an input from a particular semicircular canal nerve branches we used single constant current canal are clustered and form modular zones that represent pulses 0.2 ms; 8–12 mA across suction electrodes inner different vestibular endorgans in a manner similar to diameter 120–150 mm; see [34]. For stimulation of the retinotopic, somatotopic or tonotopic maps of other sen- VIIIth nerve we used single constant current pulses 0.2 sory systems. ms; 5–30 mA across a concentric bipolar electrode tip We analyzed these possibilities first with evoked field diameter 25 mm that was located about 2 mm more potentials recorded in vitro in the isolated frog brain. proximal than the electrodes stimulating the individual Separate electrical stimulation of individual semicircular semicircular canal nerves [34]. Constant current pulses canal nerves activated field potentials that consisted of two were produced by a stimulus isolation unit WPI A 360 at or more negative components. The spatial distribution of a repetition rate of 0.33 Hz. For extracellular recordings vestibular nerve evoked N and N field potentials, glass microelectrodes were fabricated with a horizontal 1 representing regional presynaptic N and postsynaptic puller P-87 Brown Flaming, beveled 308, 20 mm tip N response components [28], was mapped systematical- diameter and filled with 2 M sodium chloride 1–3 MV. 1 ly. We compared these results with the location of 28VN, Electrodes for intracellular recordings were filled with 2 M identified by their monosynaptic responses following elec- potassium acetate 90–120 MV or 2 M potassium chlo- trical stimulation of the horizontal, anterior vertical or ride 80–100 MV. Vertical displacements of the recording posterior vertical semicircular canal nerve branch. The electrodes were controlled with a nanostepper. Horizontal physiological response properties of these neurons had displacements were performed with a two axes micro- been described elsewhere [34]. manipulator. Preliminary parts of this study had been published in In order to standardize our results field potentials were abstract form [35]. recorded at the beginning of each experiment at the same standard recording site 0.4 mm caudal to the caudal end of the entry of the VIIIth nerve at a depth of 0.4 mm below

2. Material and methods the top of the brainstem. The stimulus threshold for the