Patterns of Canal and Otolith Afferent Input Convergence in Frog Second-Order Vestibular Neurons

Abstract

Straka, H., S. Holler, and F. Goto. Patterns of canal and otolith afferent input convergence in frog second-order vestibular neurons. J Neurophysiol 88: 2287-2301, 2002 10.1152/jn.00370.2002 were identified in the isolated frog brain by the presence of monosynaptic excitatory postsynaptic potentials (EPSPs) after separate electrical stimulation of individual vestibular nerve branches. Combinations of one macular and the three semicircular canal nerve branches or combinations of two macular nerve branches were stimulated separately in different sets of experiments. Monosynaptic EPSPs evoked from the utricle or from the lagena converged with monosynaptic EPSPs from one of the three semicircular canal organs in ϳ30% of 2°VN. Utricular afferent signals converged predominantly with horizontal canal afferent signals (74%), and lagenar afferent signals converged with anterior vertical (63%) or posterior vertical (37%) but not with horizontal canal afferent signals. This convergence pattern correlates with the coactivation of particular combinations of canal and otolith organs during natural head movements. A convergence of afferent saccular and canal signals was restricted to very few 2°VN (3%). In contrast to the considerable number of 2°VN that received an afferent input from the utricle or the lagena as well as from one of the three canal nerves (ϳ30%), smaller numbers of 2°VN (14% of each type of 2°otolith or 2°canal neuron) received an afferent input from only one particular otolith organ or from only one particular semicircular canal organ. Even fewer 2°VN received an afferent input from more than one semicircular canal or from more than one otolith nerve (ϳ7% each). Among 2°VN with afferent inputs from more than one otolith nerve, an afferent saccular nerve input was particularly rare (4 -5%). The restricted convergence of afferent saccular inputs with other afferent otolith or canal inputs as well as the termination pattern of saccular afferent fibers are compatible with a substrate vibration sensitivity of this otolith organ in frog. The ascending and/or descending projections of identified 2°VN were determined by the presence of antidromic spikes. 2°VN mediating afferent utricular and/or semicircular canal nerve signals had ascending and/or descending axons. 2°VN mediating afferent lagenar or saccular nerve signals had descending but no ascending axons. The latter result is consistent with the absence of short-latency macular signals on extraocular motoneurons during vertical linear acceleration. Comparison of data from frog and cat demonstrated the presence of a similar organization pattern of maculo-and canal-ocular reflexes in both species. I N T R O D U C T I O NComponents of linear and angular head acceleration are detected separately by the different otolith and semicircular canal organs in the labyrinth. These signals are mediated in parallel pathways by afferent nerve fibers to the vestibular nuclei, the brain stem reticular formation, and the cerebellum. Afferent nerve fibers from individual semicirc...

Development of vestibular afferent projections into the hindbrain and their central targets

“…Indeed, the location and distribution of primary vestibular neurons should not be relevant for evoking a specific response as long as primary vestibular neurons sort out their peripheral projections to topographically, and functionally distinct receptor sites and project centrally to a functionally organized output of second order neurons. This sorting of vestibular afferent input to second order vestibular neurons has been shown by Straka et al [93] despite the fact that afferent fibers emanating from different endorgans have an overlapping distribution [9]. Such a scheme of distribution is similar to dorsal root ganglion neurons whose different subpopulations, conveying different sensory information, are overlapping at the level of the ganglion [65].…”

“…It is generally agreed that, in their central representation, each endorgans has a domain of almost exclusive projection and a domain of sparse projection overlapping with other endorgans, reproducing the peripheral distribution pattern at the level of the ganglion [16,26,59,68,75]. Such a partial functional as well as anatomical overlap is best known for the frog [9,92,93]. This central overlapping pattern may be a universal functional feature of the vestibular system to converge monosynaptically afferent canal and otolith inputs [93] to integrate multiple inputs, and yet to respond in precise and finely graded fashion to unique signals (Newlands and Perachio, this volume).…”

“…Such a partial functional as well as anatomical overlap is best known for the frog [9,92,93]. This central overlapping pattern may be a universal functional feature of the vestibular system to converge monosynaptically afferent canal and otolith inputs [93] to integrate multiple inputs, and yet to respond in precise and finely graded fashion to unique signals (Newlands and Perachio, this volume).…”

Differential Dynamic Processing of Afferent Signals in Frog Tonic and Phasic Second-Order Vestibular Neurons

“…At the beginning of each experiment, presynaptic and postsynaptic field potentials evoked by separate stimulation of the labyrinthine nerve branches were recorded at a standard reference site in the vestibular nuclei to optimize the position of the stimulus electrodes and to determine the stimulus threshold ( T) for each nerve branch (Straka et al, 1997(Straka et al, , 2002. Stimulus intensities were indicated as multiples of the threshold values for the postsynaptic field potentials.…”

Second-Order Vestibular Neurons Form Separate Populations With Different Membrane and Discharge Properties

“…In addition, the frog model offers the unique opportunity to link the membrane properties of 2°VN with their anatomical location and their afferent and efferent connectivity. In particular, the spatial convergence pattern of semicircular canal and macular signals on 2°VN has been well described (Straka et al 1997(Straka et al , 2002. Almost half of the 2°VN receive convergent afferent nerve input from one macula and one canal organ in a spatially specific manner (Straka et al 2002).…”