Convergent Properties of Vestibular-Related Brain Stem Neurons in the Gerbil

2000 ◽  
Vol 83 (4) ◽  
pp. 1958-1971 ◽  
Author(s):  
Galen D. Kaufman ◽  
Michael E. Shinder ◽  
Adrian A. Perachio

Three classes of vestibular-related neurons were found in and near the prepositus and medial vestibular nuclei of alert or decerebrate gerbils, those responding to: horizontal translational motion, horizontal head rotation, or both. Their distribution ratios were 1:2:2, respectively. Many cells responsive to translational motion exhibited spatiotemporal characteristics with both response gain and phase varying as a function of the stimulus vector angle. Rotationally sensitive neurons were distributed as Type I, II, or III responses (sensitive to ipsilateral, contralateral, or both directions, respectively) in the ratios of 4:6:1. Four tested factors shaped the response dynamics of the sampled neurons: canal-otolith convergence, oculomotor-related activity, rotational Type (I or II), and the phase of the maximum response. Type I nonconvergent cells displayed increasing gains with increasing rotational stimulus frequency (0.1–2.0 Hz, 60°/s), whereas Type II neurons with convergent inputs had response gains that markedly decreased with increasing translational stimulus frequency (0.25–2.0 Hz, ±0.1 g). Type I convergent and Type II nonconvergent neurons exhibited essentially flat gains across the stimulus frequency range. Oculomotor-related activity was noted in 30% of the cells across all functional types, appearing as burst/pause discharge patterns related to the fast phase of nystagmus during head rotation. Oculomotor-related activity was correlated with enhanced dynamic range compared with the same category that had no oculomotor-related response. Finally, responses that were in-phase with head velocity during rotation exhibited greater gains with stimulus frequency increments than neurons with out-of-phase responses. In contrast, for translational motion, neurons out of phase with head acceleration exhibited low-pass characteristics, whereas in-phase neurons did not. Data from decerebrate preparations revealed that although similar response types could be detected, the sampled cells generally had lower background discharge rates, on average one-third lower response gains, and convergent properties that differed from those found in the alert animals. On the basis of the dynamic response of identified cell types, we propose a pair of models in which inhibitory input from vestibular-related neurons converges on oculomotor neurons with excitatory inputs from the vestibular nuclei. Simple signal convergence and combinations of different types of vestibular labyrinth information can enrich the dynamic characteristics of the rotational and translational vestibuloocular responses.

1994 ◽  
Vol 71 (6) ◽  
pp. 2087-2092 ◽  
Author(s):  
B. J. Yates ◽  
A. D. Miller

1. To study the properties of vestibulosympathetic reflexes we recorded outflow from the splanchnic nerve during natural vestibular stimulation in multiple vertical planes in decerebrate cats. Most of the animals were cerebellectomized, although some responses were recorded in cerebellum-intact preparations. Vestibular stimulation was produced by rotating the head in animals whose upper cervical dorsal roots were transected to remove inputs from neck receptors; a baroreceptor denervation and vagotomy were also performed to remove visceral inputs. 2. The plane of head rotation that produced maximal modulation of splanchnic nerve activity (response vector orientation) was measured at 0.2–0.5 Hz. The dynamics of the response were then studied with sinusoidal (0.05- to 1-Hz) stimuli aligned with this orientation. 3. Typically, maximal modulation of splanchnic nerve outflow was elicited by head rotations in a plane near pitch; nose-up rotations produced increased outflow and nose-down rotations reduced nerve discharges. The gains of the responses remained relatively constant across stimulus frequencies and the phases were consistently near stimulus position, like regularly firing otolith afferents. Similar response dynamics were recorded in cerebellectomized and cerebellum-intact animals. 4. The splanchnic nerve responses to head rotation could be abolished by microinjections of the excitotoxin kainic acid into the medial and inferior vestibular nuclei, which is concordant with the responses resulting from activation of vestibular receptors. 5. The properties fo vestibulosympathetic reflexes recorded from the splanchnic nerve support the hypothesis that the vestibular system participates in compensating for posturally related changes in blood pressure.


1979 ◽  
Vol 88 (5) ◽  
pp. 667-675 ◽  
Author(s):  
Richard R. Gacek

The modern neuroanatomical technique of using a retrograde axoplasmic tracer (horseradish peroxidase) to label neurons has aided the revelation of several important connections in the vestibular system. The organization of the oculomotor nucleus and the existence of an interneuron in the abducens nucleus have importance in understanding some ocular disorders. A detailed description of the location of vestibulo-ocular neurons to individual extraocular muscles is now available which may provide a basis for understanding how these reflexes function normally and abnormally. Interconnections between the vestibular nuclei are provided by commissural neurons located in the superior, medial and group Y nuclei. These projections are probably of importance in vestibular compensation. A possible hypothesis of vestibular hair cell projection suggests that type I cells project over vestibulo-ocular neurons while type II cells project over commissural pathways.


2002 ◽  
Vol 88 (6) ◽  
pp. 3279-3292 ◽  
Author(s):  
Jay M. Goldberg ◽  
Alan M. Brichta

Controlled currents were used to study possible functions of voltage-sensitive, outwardly rectifying conductances. Results were interpreted with linearized Hodgkin-Huxley theory. Because of their more hyperpolarized resting potentials and lower impedances, type I hair cells require larger currents to be depolarized to a given voltage than do type II hair cells. “Fast” type II cells, so-called because of the fast activation of their outward currents, show slightly underdamped responses to current steps with resonant (best) frequencies of 40–85 Hz, well above the bandwidth of natural head movements. Reflecting their slower activation kinetics, type I and “slow” type II cells have best frequencies of 15–30 Hz and are poorly tuned, being critically damped or overdamped. Linearized theory identified the factors responsible for tuning quality. Our fast type II hair cells show only modestly underdamped responses because their steady-state I-V curves are not particularly steep. The even poorer tuning of our type I and slow type II cells can be attributed to their slow activation kinetics and large conductances. To study how ionic currents shape response dynamics, we superimposed sinusoidal currents of 0.1–100 Hz on a small depolarizing steady current intended to simulate resting conditions in vivo. The steady current resulted in a slow inactivation, most pronounced in fast type II cells and least pronounced in type I cells. Because of inactivation, fast type II cells have nearly passive response dynamics with low-frequency gains of 500–1,000 MΩ. In contrast, type I and slow type II cells show active components in the vestibular bandwidth and low-frequency gains of 20–100 and 100–500 MΩ, respectively. As there are no differences in the responses to sinusoidal currents for fast type II cells from the torus and planum, voltage-sensitive currents are unlikely to be responsible for the large differences in gains and response dynamics of afferents innervating these two regions of the peripheral zone. The low impedances and active components of type I cells may be related to the low gains and modestly phasic response dynamics of calyx-bearing afferents.


2005 ◽  
Vol 94 (4) ◽  
pp. 2379-2390 ◽  
Author(s):  
M. F. Kubke ◽  
Y. Yazaki-Sugiyama ◽  
R. Mooney ◽  
J. M. Wild

Learned vocalizations, such as bird song, require intricate coordination of vocal and respiratory muscles. Although the neural basis for this coordination remains poorly understood, it likely includes direct synaptic interactions between respiratory premotor neurons and vocal motor neurons. In birds, as in mammals, the medullary nucleus retroambigualis (RAm) receives synaptic input from higher level respiratory and vocal control centers and projects to a variety of targets. In birds, these include vocal motor neurons in the tracheosyringeal part of the hypoglossal motor nucleus (XIIts), other respiratory premotor neurons, and expiratory motor neurons in the spinal cord. Although various cell types in RAm are distinct in their anatomical projections, their electrophysiological properties remain unknown. Furthermore, although prior studies have shown that RAm provides both excitatory and inhibitory input onto XIIts motor neurons, the identity of the cells in RAm providing either of these inputs remains to be established. To characterize the different RAm neuron types electrophysiologically, we used intracellular recordings in a zebra finch brain stem slice preparation. Based on numerous differences in intrinsic electrophysiological properties and a principal components analysis, we identified two distinct RAm neuron types (types I and II). Antidromic stimulation methods and intracellular staining revealed that type II neurons, but not type I neurons, provide bilateral synaptic input to XIIts. Paired intracellular recordings in RAm and XIIts further indicated that type II neurons with a hyperpolarization-dependent bursting phenotype are a potential source of inhibitory input to XIIts motor neurons. These results indicate that electrically distinct cell types exist in RAm, affording physiological heterogeneity that may play an important role in respiratory–vocal signaling.


1993 ◽  
Vol 69 (6) ◽  
pp. 2039-2055 ◽  
Author(s):  
G. A. Bush ◽  
A. A. Perachio ◽  
D. E. Angelaki

1. Extracellular recordings were made in and around the medial vestibular nuclei in decerebrated rats. Neurons were functionally identified according to their semicircular canal input on the basis of their responses to angular head rotations around the yaw, pitch, and roll head axes. Those cells responding to angular acceleration were classified as either horizontal semicircular canal-related (HC) or vertical semicircular canal-related (VC) neurons. The HC neurons were further characterized as either type I or type II, depending on the direction of rotation producing excitation. Cells that lacked a response to angular head acceleration, but exhibited sensitivity to a change in head position, were classified as purely otolith organ-related (OTO) neurons. All vestibular neurons were then tested for their response to sinusoidal linear translation in the horizontal head plane. 2. Convergence of macular and canal inputs onto central vestibular nuclei neurons occurred in 73% of the type I HC, 79% of the type II HC, and 86% of the VC neurons. Out of the 223 neurons identified as receiving macular input, 94 neurons were further studied, and their spatiotemporal response properties to sinusoidal stimulation with pure linear acceleration were quantified. Data were obtained from 33 type I HC, 22 type II HC, 22 VC, and 17 OTO neurons. 3. For each neuron the angle of the translational stimulus vector was varied by 15, 30, or 45 degrees increments in the horizontal head plane. In all tested neurons, a direction of maximum sensitivity was identified. An interesting difference among neurons was their response to translation along the direction perpendicular to that that produced the maximum response ("null" direction). For the majority of neurons tested, it was possible to evoke a nonzero response during stimulation along the null direction always had response phases that varied as a function of stimulus direction. 4. These spatiotemporal response properties were quantified in two independent ways. First, the data were evaluated on the basis of the traditional one-dimensional principle governed by the "cosine gain rule" and constant response phase at different stimulus orientations. Second, the response gain and phase values that were empirically determined for each orientation of the applied linear stimulus vector were fitted on the basis of a newly developed formalism that treats neuronal responses as exhibiting two-dimensional spatial sensitivity. Thus two response vectors were determined for each neuron on the basis of its response gain and phase at different stimulus directions in the horizontal head plane.(ABSTRACT TRUNCATED AT 400 WORDS)


2000 ◽  
Vol 83 (3) ◽  
pp. 1202-1223 ◽  
Author(s):  
Alan M. Brichta ◽  
Jay M. Goldberg

The turtle posterior crista consists of two hemicristae. Each hemicrista extends from the planum semilunatum to the nonsensory torus and includes a central zone (CZ) surrounded by a peripheral zone (PZ). Type I and type II hair cells are found in the CZ and are innervated by calyx, dimorphic and bouton afferents. Only type II hair cells and bouton fibers are found in the PZ. Units were intraaxonally labeled in a half-head preparation. Bouton (B) units could be near the planum (BP), near the torus (BT), or in midportions of a hemicrista, including the PZ and CZ. Discharge properties of B units vary with longitudinal position in a hemicrista but not with morphological features of their peripheral terminations. BP units are regularly discharging and have small gains and small phase leads re angular head velocity. BT units are irregular and have large gains and large phase leads. BM units have intermediate properties. Calyx (C) and dimorphic (D) units have similar discharge properties and were placed into a single calyx-bearing (CD) category. While having an irregular discharge resembling BT units, CD units have gains and phases similar to those of BM units. Rather than any single discharge property, it is the relation between discharge regularity and either gain or phase that makes CD units distinctive. Multivariate statistical formulas were developed to infer a unit's morphological class (B or CD) and longitudinal position solely from its discharge properties. To verify the use of the formulas, discharge properties were compared for units recorded intraaxonally or extracellularly in the half-head or extracellularly in intact animals. Most B units have background rates of 10–30 spikes/s. The CD category was separated into CD-high and CD-low units with background rates above or below 5 spikes/s, respectively. CD-low units have lower gains and phases and are located nearer the planum than CD-high units. In their response dynamics over a frequency range from 0.01–3 Hz, BP units conform to an overdamped torsion-pendulum model. Other units show departures from the model, including high-frequency gain increases and phase leads. The longitudinal gradient in the physiology of turtle B units resembles a similar gradient in the anamniote crista. In many respects, turtle CD units have discharge properties resembling those of calyx-bearing units in the mammalian central zone.


2002 ◽  
Vol 88 (6) ◽  
pp. 3518-3533 ◽  
Author(s):  
J. David Dickman ◽  
Dora E. Angelaki

Sensory signal convergence is a fundamental and important aspect of brain function. Such convergence may often involve complex multidimensional interactions as those proposed for the processing of otolith and semicircular canal (SCC) information for the detection of translational head movements and the effective discrimination from physically congruent gravity signals. In the present study, we have examined the responses of primate rostral vestibular nuclei (VN) neurons that do not exhibit any eye movement-related activity using 0.5-Hz translational and three-dimensional (3D) rotational motion. Three distinct neural populations were identified. Approximately one-fourth of the cells exclusively encoded rotational movements (canal-only neurons) and were unresponsive to translation. The canal-only central neurons encoded head rotation in SCC coordinates, exhibited little orthogonal canal convergence, and were characterized with significantly higher sensitivities to rotation as compared to primary SCC afferents. Another fourth of the neurons modulated their firing rates during translation (otolith-only cells). During rotations, these neurons only responded when the axis of rotation was earth-horizontal and the head was changing orientation relative to gravity. The remaining one-half of VN neurons were sensitive to both rotations and translations (otolith + canal neurons). Unlike primary otolith afferents, however, central neurons often exhibited significant spatiotemporal (noncosine) tuning properties and a wide variety of response dynamics to translation. To characterize the pattern of SCC inputs to otolith + canal neurons, their rotational maximum sensitivity vectors were computed using exclusively responses during earth-vertical axis rotations (EVA). Maximum sensitivity vectors were distributed throughout the 3D space, suggesting strong convergence from multiple SCCs. These neurons were also tested with earth-horizontal axis rotations (EHA), which would activate both vertical canals and otolith organs. However, the recorded responses could not be predicted from a linear combination of EVA rotational and translational responses. In contrast, one-third of the neurons responded similarly during EVA and EHA rotations, although a significant response modulation was present during translation. Thus this subpopulation of otolith + canal cells, which included neurons with either high- or low-pass dynamics to translation, appear to selectively ignore the component of otolith-selective activation that is due to changes in the orientation of the head relative to gravity. Thus contrary to primary otolith afferents and otolith-only central neurons that respond equivalently to tilts relative to gravity and translational movements, approximately one-third of the otolith + canal cells seem to encode a true estimate of the translational component of the imposed passive head and body movement.


1979 ◽  
Vol 42 (5) ◽  
pp. 1479-1493 ◽  
Author(s):  
R. Budelli ◽  
O. Macadar

1. We classified the utricular afferents on the basis of their spontaneous acitivity and responses to tilts and vibrations. 2. Type I afferents fire spontaneously in a regular pattern; their responses to tilts consist of a phasic-tonic change in firing rate. They may respond to vibrations by increasing or decreasing their rate and show no adaptation. 3. The spontaneous activity and the responses to tilts of type II are similar to those observed in type I afferents. The differences become apparent when the preparation is subjected to a vibrational stimulus, since type II neurons increase their firing rate regardless of the stimulus frequency and show adaptation. 4. Type III neurons have no spontaneous activity. They respond to tilts by firing during the transition from one position to the other. They respond to a vibrational stimulus with maintained firing and show no adaptation. 5. We studied the dynamic responses of each type of neuron. We used sensitivity curves for the study of type III afferents and proposed a statistical method to define gain curves for the study of the other types. 6. The gain curves generated by type I neurons reach their maximum at frequencies of stimulation close to the spontaneous rate of firing. 7. In the gain curves of type II afferents the maximum corresponds to frequencies higher than their spontaneous activity. 8. Sensitivity curves and gain curves give similar results for type III fibers. The sensitivity curves of these afferents were classified into four subtypes. 9. We studied the responses of the three types of afferents to bursts of sinusoidal vibrations. 10. We concluded that the properties of types I and II fibers are fit to carry information about movements and position of the head, but also transmit acoustical information. Type III fibers are more adapted to provide information about acoustical stimuli, but can also convey information about head movements.


1982 ◽  
Vol 11 (1) ◽  
pp. 25-34 ◽  
Author(s):  
Thomas A. Grigalunas ◽  
Craig A. Ascari

This paper summarizes some results of a Sea Grant-funded economic input-output study of marine-related activity in the Southern New England Marine Region. Data were obtained from 390 personal interviews; in addition, a wealth of secondary data was used. Type I and Type II income and employment multipliers were estimated for each of the nineteen marine-related industries included in the model. The results provide a basis to assist analysts concerned with assessing the impacts on regional income and employment of marine-related policies or developments proposed for the Region.


2002 ◽  
Vol 87 (1) ◽  
pp. 322-332 ◽  
Author(s):  
Terry Crow ◽  
Lian-Ming Tian

The synaptic interactions between photoreceptors in the eye and second-order neurons in the optic ganglion of the nudibranch mollusk Hermissenda are well characterized. However, the higher-order neural circuitry of the visual system, consisting of cerebropleural interneurons that receive synaptic input from photoreceptors and project to pedal motor neurons that mediate visually guided behaviors, is only partially understood. In this report we have examined the central projections of two identified classes of cerebropleural interneurons that receive excitatory or inhibitory synaptic input from identified photoreceptors. The classification of the interneurons was based on both morphological and electrophysiological criteria. Type I interneurons received monosynaptic excitatory or inhibitory synaptic input from identified photoreceptors and projected to postsynaptic targets within the cerebropleural ganglion. Type II interneurons, characterized here for the first time, received polysynaptic excitatory or inhibitory synaptic input from identified photoreceptors and projected to postsynaptic targets in either the ipsilateral pedal ganglion or the contralateral cerebropleural ganglion. Type I interneurons exhibited unique intraganglionic projections to different regions of the cerebropleural ganglion, depending on whether they received excitatory or inhibitory synaptic input from identified photoreceptors. Type I interneurons that received monosynaptic excitatory input from identified B photoreceptors terminated near the cerebropleural commissure and had multiple regions of varicosities located at branches that projected from the primary axon. Type I interneurons that received monosynaptic inhibitory input from identified B photoreceptors projected to the anterior cerebropleural ganglion and exhibited varicosities localized to the terminal region of the primary axonal process. Type II interneurons that received polysynaptic inhibitory input from identified photoreceptors projected to the contralateral cerebropleural ganglion. Most type II interneurons that projected to the pedal ganglia received polysynaptic excitatory input from identified photoreceptors. These results indicate that there is at least one additional interneuron in the higher-order visual circuit between type I interneurons and pedal motor neurons responsible for the generation of phototactic locomotion in Hermissenda.


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