Anticipation in the Rodent Head Direction System Can Be Explained by an Interaction of Head Movements and Vestibular Firing Properties

2007 ◽  
Vol 98 (4) ◽  
pp. 1883-1897 ◽  
Author(s):  
Matthijs A. A. van der Meer ◽  
James J. Knierim ◽  
D. Yoganarasimha ◽  
Emma R. Wood ◽  
Mark C. W. van Rossum
Keyword(s):  
Vestibular Nucleus ◽  
Passive Movement ◽  
Head Movements ◽  
Medial Vestibular Nucleus ◽  
Electrophysiological Recording ◽  
Head Direction ◽  
Movement Data ◽  
Behavioral Variables ◽  
Firing Properties ◽  
Functional Circuitry

The rodent head-direction (HD) system, which codes for the animal's head direction in the horizontal plane, is thought to be critically involved in spatial navigation. Electrophysiological recording studies have shown that HD cells can anticipate the animal's HD by up to 75–80 ms. The origin of this anticipation is poorly understood. In this modeling study, we provide a novel explanation for HD anticipation that relies on the firing properties of neurons afferent to the HD system. By incorporating spike rate adaptation and postinhibitory rebound as observed in medial vestibular nucleus neurons, our model produces realistic anticipation on a large corpus of rat movement data. In addition, HD anticipation varies between recording sessions of the same cell, between active and passive movement, and between different studies. Such differences do not appear to be correlated with behavioral variables and cannot be accounted for using earlier models. In the present model, anticipation depends on the power spectrum of the head movements. By direct comparison with recording data, we show that the model explains 60–80% of the observed anticipation variability. We conclude that HD afferent dynamics and the statistics of rat head movements are important in generating HD anticipation. This result contributes to understanding the functional circuitry of the HD system and has methodological implications for studies of HD anticipation.

Physiological and Anatomical Properties of Mouse Medial Vestibular Nucleus Neurons Projecting to the Oculomotor Nucleus

2006 ◽  
Vol 95 (5) ◽  
pp. 3012-3023 ◽  
Author(s):  
Chris Sekirnjak ◽  
Sascha du Lac
Keyword(s):  
Vestibular Nucleus ◽  
High Sensitivity ◽  
Current Injection ◽  
Head Movements ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Oculomotor Nucleus ◽  
Response Dynamics ◽  
Tracer Injection ◽  
Membrane Hyperpolarization

Neurons in the medial vestibular nucleus (MVN) vary in their projection patterns, responses to head movement, and intrinsic firing properties. To establish whether neurons that participate in the vestibulo-ocular reflex (VOR) have distinct intrinsic physiological properties, oculomotor nucleus (OMN)–projecting neurons were identified in mouse brainstem slices by fluorescent retrograde labeling from the oculomotor complex and targeted for patch-clamp recordings. Such neurons were located in the magnocellular portion of the MVN contralateral to tracer injection, were mostly multipolar, and had soma diameters of around 20 μm. They fired spontaneous action potentials at rates higher than those of other MVN neurons and their spikes were of unusually short duration. OMN-projecting neurons responded to 1-s intracellular current injection with exceptionally high firing rates of >500 spikes/s. Their current–firing relationship was highly linear, with weak firing response adaptation during steady depolarization and little postinhibitory rebound firing after membrane hyperpolarization. Their firing responses were approximately in phase with sinusoidal current injection. The response dynamics of OMN-projecting neurons could be simulated with a simple integrate-and-fire model modified with the addition of small adaptation and rebound conductances. These findings indicate that the membrane properties of OMN-projecting neurons allow them to respond to head movements reliably and with high sensitivity but without substantially altering input dynamics.

Unilateral Labyrinthectomy Modifies the Membrane Properties of Contralesional Vestibular Neurons

2004 ◽  
Vol 92 (3) ◽  
pp. 1668-1684 ◽  
Author(s):  
Mathieu Beraneck ◽  
Erwin Idoux ◽  
Atsuhiko Uno ◽  
Pierre-Paul Vidal ◽  
Lee E. Moore ◽  
...  
Keyword(s):  
Type A ◽  
Head Movements ◽  
Vestibular Compensation ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Type B ◽  
Response Dynamics ◽  
Vestibular Reflexes ◽  
Unilateral Labyrinthectomy ◽  
Firing Properties

Vestibular compensation after a unilateral labyrinthectomy leads to nearly complete disappearance of the static symptoms triggered by the lesion. However, the dynamic vestibular reflexes associated with head movements remain impaired. Because the contralesional labyrinth plays a prominent role in the generation of these dynamic responses, intracellular recordings of contralesional medial vestibular nucleus neurons (MVNn) were done after 1 mo of compensation. Their firing properties and cell type were characterized at rest, and their response dynamics investigated using step, ramp, and sinusoidal current stimulations. The sensitivity of the contralesional MVNn firing rates to applied current was increased, which, along with increased phase leads, suggests that significant changes in active conductances occurred. We found an increased proportion of the phasic type B neurons relative to the tonic type A neurons in the contralesional MVN. In addition, the remaining contralesional type A MVNn response dynamics tended to approach those of type B MVNn. Thus the contralesional MVNn in general showed more phasic response dynamics than those of control MVNn. Altogether, the firing properties of MVNn are differentially modified on the ipsilesional and contralesional sides of the brain stem 1 mo after unilateral labyrinthectomy. Ipsilesional MVNn acquire more “type A–like” tonic membrane properties, which would contribute to the stabilization of the spontaneous activity that recovers in the deafferented neurons during vestibular compensation. The bilateral increase in the sensitivity of MVNn and the acquisition of more “B-like” phasic membrane properties by contralesional MVNn should promote the restoration of the vestibular reflexes generated by the remaining, contralesional labyrinth.

scholarly journals Passive Movements of the Head Do Not Abolish Anticipatory Firing Properties of Head Direction Cells

2005 ◽  
Vol 93 (3) ◽  
pp. 1304-1316 ◽  
Author(s):  
Joshua P. Bassett ◽  
Michaël B. Zugaro ◽  
Gary M. Muir ◽  
Edward J. Golob ◽  
Robert U. Muller ◽  
...  
Keyword(s):  
Thalamic Nucleus ◽  
Passive Movement ◽  
Efference Copy ◽  
Time Interval ◽  
Head Direction ◽  
Preferred Direction ◽  
Cell Firing ◽  
Firing Properties ◽  
Passive Movements ◽  
Active Contribution

Neurons in the anterior dorsal thalamic nucleus (ADN) of the rat selectively discharge in relation to the animal's head direction (HD) in the horizontal plane. Temporal analyses of cell firing properties reveal that their discharge is optimally correlated with the animal's future directional heading by ∼24 ms. Among the hypotheses proposed to explain this property is that ADN HD cells are informed of future head movement via motor efference copy signals. One prediction of this hypothesis is that when the rat's head is moved passively, the anticipatory time interval (ATI) will be attenuated because the motor efference signal reflects only the active contribution to the movement. The present study tested this hypothesis by loosely restraining the animal and passively rotating it through the cell's preferred direction. Contrary to our prediction, we found that ATI values did not decrease during passive movement but in fact increased significantly. HD cells in the postsubiculum did not show the same effect, suggesting independence between the two sites with respect to anticipatory firing. We conclude that it is unlikely that a motor efference copy signal alone is responsible for generating anticipatory firing in ADN HD cells.

Excitation and inhibition of rat medial vestibular nucleus neurones by 5-hydroxytryptamine

1993 ◽  
Vol 93 (2) ◽  
Author(s):  
A.R. Johnston ◽  
Bridin Murnion ◽  
D.S. McQueen ◽  
M.B. Dutia
Keyword(s):  
Vestibular Nucleus ◽  
Medial Vestibular Nucleus

Plasticity of γ-aminobutyrate receptors in the medial vestibular nucleus of rat after inferior cerebellar peduncle transection

2002 ◽  
Vol 12 (1) ◽  
pp. 1-14
Author(s):  
Yizhe Sun ◽  
Donald A. Godfrey ◽  
Allan M. Rubin
Keyword(s):  
Vestibular Nucleus ◽  
Brain Slices ◽  
Medial Vestibular Nucleus ◽  
Grouped Data ◽  
Spontaneous Firing ◽  
Gaba A ◽  
Endogenous Gaba ◽  
Single Unit Recordings ◽  
Cerebellar Peduncle ◽  
Inferior Cerebellar Peduncle

Extracellular single unit recordings were made from regularly discharging medial vestibular nucleus neurons in brain slices from control rats and from rats surviving 7 days after bilateral transection of the inferior cerebellar peduncle. Decreases in firing rate during perfusion with the Îş-aminobutyric acid (GABA) agonists, muscimol (GABA A ) and baclofen (GABA B ), were greater in lesioned rats than in control rats. For the grouped data, the half-maximally-effective concentrations of muscimol and baclofen were 3.2 µM, as compared with 19.6 µM for control, and 0.8 µM, as compared with 2.7 µM for control, respectively. The antagonists bicuculline (GABA A ) and 2-OH-saclofen (GABA B ) only minimally affected the spontaneous firing rates of neurons in lesioned rats, significantly less than in control rats. The data suggest that the decreases of endogenous GABA levels in the medial vestibular nucleus after inferior cerebellar peduncle transection are accompanied by up-regulation of GABA A and, to a lesser extent, GABA B receptors.

Unilateral labyrinthectomy induced changes on GDNF receptor complex proteins in the rat medial vestibular nuclei

2007 ◽  
Vol 16 (4-5) ◽  
pp. 171-177
Author(s):  
Adrian Lozada ◽  
Kaj Karlstedt ◽  
Pertti Panula ◽  
Antti A. Aarnisalo
Keyword(s):  
Mrna Expression ◽  
Vestibular Nucleus ◽  
Medial Vestibular Nucleus ◽  
Receptor Complex ◽  
Trophic Effect ◽  
Expression Levels ◽  
Protein Levels ◽  
Unilateral Labyrinthectomy ◽  
Ganglion Neurons ◽  
Mrna Expression Levels

In the auditory periphery, GDNF has been shown to have a trophic effect to spiral ganglion neurons, both during development and in adult animals. We have studied the effect of unilateral labyrinthectomy (UL) on protein levels and expression of GDNF multicomponent receptor complex: the ret tyrosine kinase and coreceptor GFRα-1 in the medial vestibular nucleus of the adult rat. GFRα-1 protein levels display an increasing trend in ipsilateral medial vestibular nucleus culminating at 48 h post UL. On the other hand, GFRα-1 mRNA expression levels in ipsi- and contralateral medial vestibular nucleus show a steadily decreasing trend that is significant at 1 week post-lesion. Protein levels for c-Ret isoforms also show an initial bilateral decreasing trend that ceases at 48 h in ipsilateral medial vestibular nucleus but persists on the contralateral side. c-Ret mRNA expression levels show a significant decrease at 4 h post UL followed by another significant decrease 1 week post UL. Our data would suggest that neurotrophins belonging to the GDNF family are involved in this model of post-lesional CNS plasticity.

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