Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration

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)

2016 ◽  
Vol 116 (4) ◽  
pp. 1871-1884 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei ◽  
David Morgan ◽  
Hongge Luan

After vestibular labyrinth injury, behavioral measures of vestibular performance recover to variable degrees (vestibular compensation). Central neuronal responses after unilateral labyrinthectomy (UL), which eliminates both afferent resting activity and sensitivity to movement, have been well-studied. However, unilateral semicircular canal plugging (UCP), which attenuates angular-velocity detection while leaving afferent resting activity intact, has not been extensively studied. The current study reports response properties of yaw-sensitive non-eye-movement rhesus macaque vestibular neurons after compensation from UCP. The responses at a series of frequencies (0.1–2 Hz) and peak velocities (15–210°/s) were compared between neurons recorded before and at least 6 wk after UCP. The gain (sp/s/°/s) of central type I neurons (responding to ipsilateral yaw rotation) on the side of UCP was reduced relative to normal controls at 0.5 Hz, ±60°/s [0.48 ± 0.30 (SD) normal, 0.32 ± 0.15 ipsilesion; 0.44 ± 0.2 contralesion]. Type II neurons (responding to contralateral yaw rotation) after UCP have reduced gain (0.40 ± 0.27 normal, 0.35 ± 0.25 ipsilesion; 0.25 ± 0.18 contralesion). The difference between responses after UCP and after UL is primarily the distribution of type I and type II neurons in the vestibular nuclei (type I neurons comprise 66% in vestibular nuclei normally; 51% ipsilesion UCP; 59% contralesion UCP; 38% ipsilesion UL; 65% contralesion UL) and the magnitude of the responses of type II neurons ipsilateral to the lesion. These differences suggest that the need to compensate for unilateral loss of resting vestibular nerve activity after UL necessitates a different strategy for recovery of dynamic vestibular responses compared to after UCP.


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.


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.


1996 ◽  
Vol 75 (5) ◽  
pp. 2117-2123 ◽  
Author(s):  
K. J. Rennie ◽  
A. J. Ricci ◽  
M. J. Correia

1. Membrane potential responses of dissociated gerbil type I semicircular canal hair cells to current injections in whole cell current-clamp have been measured. The input resistance of type I cells was 21.4 +/- 14.3 (SD) M omega, (n = 25). Around the zero-current potential (Vz = -66.6 +/- 9.3 mV, n = 25), pulsed current injections (from approximately -200 to 750 pA) produced only small-amplitude, pulse-like changes in membrane potential. 2. Injecting constant current to hyperpolarize the membrane to around -100 mV resulted in a approximately 10-fold increase in membrane resistance. Current pulses superimposed on this constant hyperpolarization produced larger and more complex membrane potential changes. Depolarizing currents > or = 200 pA caused a rapid transient peak voltage before a plateau. 3. Membrane voltage was able to faithfully follow sine-wave current injections around Vz over the range 1-1,000 Hz with < 25% attenuation at 1 kHz. A previously described K conductance, IKI, which is active at Vz, produces the low input resistance and frequency response. This was confirmed by pharmacologically blocking IKI. This conductance, present in type I cells but not type II hair cells, would appear to confer on type I cells a lower gain, but a much broader bandwidth at Vz, than seen in type II cells.


1997 ◽  
Vol 77 (5) ◽  
pp. 2549-2572 ◽  
Author(s):  
Jiang Ding ◽  
Herbert F. Voigt

Ding, Jiang and Herbert F. Voigt. Intracellular response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil. J. Neurophysiol. 77: 2549–2572, 1997. Intracellular recording experiments on the dorsal cochlear nuclei of unanesthetized decerebrate gerbils were conducted. Acceptable recordings were those in which resting potentials were −50 mV or less and action potentials (APs) were ≥40 mV. Responses to short-duration tones and noise, and to current pulses delivered via recording electrodes, were acquired. Units were classified according to the response map scheme (types I–IV). Ninety-two acceptable recordings were made. Most units had simple APs (simple-spiking units); nine units had both simple and complex APs, which are bursts of spikes embedded on slow, transient depolarizations (complex-spiking units). Of 83 simple-spiking units, 46 were classified as follows: type I/III (9 units), type II (9 units), type III (25 units), type IV (2 units), and type IV-T (1 unit). One complex-spiking unit was classifiable (a type III unit); six were unclassifiable because of weak acoustic responses. Classifying 39 other simple-spiking units and 2 complex-spiking units was impossible, because they were either injured or lost before sufficient data were acquired. Many simple-spiking units showed depolarization or hyperpolarization (∼5–10 mV) during acoustic stimulation; some were hyperpolarized during the stimulus-off period. Type I/III units were not hyperpolarized during off-best-frequency (off-BF) stimulation. In contrast, many type II units were hyperpolarized by off-BF frequencies, suggesting that they received strong inhibitory sideband inputs. When inhibited, some type III units were hyperpolarized. Type IV units were hyperpolarized during inhibition even at low levels (<60 dB SPL); sustained depolarizations occurred only at higher levels, suggesting that they receive strong inhibitory and weak excitatory inputs. Several intracellular response properties were statistically different from those of extracellularly recorded units. Intracellularly recorded type II units had higher thresholds and lower maximum BF-driven and noise-driven rates than their extracellularly recorded counterparts. Type I/III units recorded intracellularly had lower maximum BF-driven rates. Type III units recorded intracellularly had higher maximum noise rates compared with those recorded extracellularly. Weaker acoustic responses most likely result from membrane disruption, but heightened responses may be related to weakened chloride-channel-dependent inhibition due to altered driving forces resulting from KCl leakage. Firing rates of simple-spiking units increased monotonically with increasing levels of depolarizing current pulses. In contrast, many complex-spiking units responded nonmonotonically to depolarizing current injection. The monotonic rate-versus-current curves and the nonmonotonic rate-versus-sound level curves of type IV and III units suggest that the acoustic behavior is the result of extrinsic inhibitory inputs and not due solely to intrinsic membrane properties.


2005 ◽  
Vol 451 (2) ◽  
pp. 395-408 ◽  
Author(s):  
Sergio Masetto ◽  
Valeria Zampini ◽  
Giampiero Zucca ◽  
Paolo Valli

Author(s):  
Ronald S. Weinstein ◽  
N. Scott McNutt

The Type I simple cold block device was described by Bullivant and Ames in 1966 and represented the product of the first successful effort to simplify the equipment required to do sophisticated freeze-cleave techniques. Bullivant, Weinstein and Someda described the Type II device which is a modification of the Type I device and was developed as a collaborative effort at the Massachusetts General Hospital and the University of Auckland, New Zealand. The modifications reduced specimen contamination and provided controlled specimen warming for heat-etching of fracture faces. We have now tested the Mass. General Hospital version of the Type II device (called the “Type II-MGH device”) on a wide variety of biological specimens and have established temperature and pressure curves for routine heat-etching with the device.


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