scholarly journals Vestibular nucleus neurons respond to hindlimb movement in the decerebrate cat

2014 ◽  
Vol 111 (12) ◽  
pp. 2423-2432 ◽  
Author(s):  
Milad S. Arshian ◽  
Candace E. Hobson ◽  
Michael F. Catanzaro ◽  
Daniel J. Miller ◽  
Sonya R. Puterbaugh ◽  
...  

The vestibular nuclei integrate information from vestibular and proprioceptive afferents, which presumably facilitates the maintenance of stable balance and posture. However, little is currently known about the processing of sensory signals from the limbs by vestibular nucleus neurons. This study tested the hypothesis that limb movement is encoded by vestibular nucleus neurons and described the changes in activity of these neurons elicited by limb extension and flexion. In decerebrate cats, we recorded the activity of 70 vestibular nucleus neurons whose activity was modulated by limb movements. Most of these neurons (57/70, 81.4%) encoded information about the direction of hindlimb movement, while the remaining neurons (13/70, 18.6%) encoded the presence of hindlimb movement without signaling the direction of movement. The activity of many vestibular nucleus neurons that responded to limb movement was also modulated by rotating the animal's body in vertical planes, suggesting that the neurons integrated hindlimb and labyrinthine inputs. Neurons whose firing rate increased during ipsilateral ear-down roll rotations tended to be excited by hindlimb flexion, whereas neurons whose firing rate increased during contralateral ear-down tilts were excited by hindlimb extension. These observations suggest that there is a purposeful mapping of hindlimb inputs onto vestibular nucleus neurons, such that integration of hindlimb and labyrinthine inputs to the neurons is functionally relevant.

2016 ◽  
Vol 116 (4) ◽  
pp. 1785-1794 ◽  
Author(s):  
Andrew A. McCall ◽  
Derek M. Miller ◽  
William M. DeMayo ◽  
George H. Bourdages ◽  
Bill J. Yates

The limbs constitute the sole interface with the ground during most waking activities in mammalian species; it is therefore expected that somatosensory inputs from the limbs provide important information to the central nervous system for balance control. In the decerebrate cat model, the activity of a subset of neurons in the vestibular nuclei (VN) has been previously shown to be modulated by hindlimb movement. However, decerebration can profoundly alter the effects of sensory inputs on the activity of brain stem neurons, resulting in epiphenomenal responses. Thus, before this study, it was unclear whether and how somatosensory inputs from the limb affected the activity of VN neurons in conscious animals. We recorded brain stem neuronal activity in the conscious cat and characterized the responses of VN neurons to flexion and extension hindlimb movements and to whole body vertical tilts (vestibular stimulation). Among 96 VN neurons whose activity was modulated by vestibular stimulation, the firing rate of 65 neurons (67.7%) was also affected by passive hindlimb movement. VN neurons in conscious cats most commonly encoded hindlimb movement irrespective of the direction of movement ( n = 33, 50.8%), in that they responded to all flexion and extension movements of the limb. Other VN neurons overtly encoded information about the direction of hindlimb movement ( n = 27, 41.5%), and the remainder had more complex responses. These data confirm that hindlimb somatosensory and vestibular inputs converge onto VN neurons of the conscious cat, suggesting that VN neurons integrate somatosensory inputs from the limbs in computations that affect motor outflow to maintain balance.


2013 ◽  
Vol 27 (S1) ◽  
Author(s):  
Milad S Arshian ◽  
Sonya R Puterbaugh ◽  
Lucy A Cotter ◽  
Bill J Yates ◽  
Andrew A McCall

1980 ◽  
Vol 44 (5) ◽  
pp. 922-936 ◽  
Author(s):  
L. Kubin ◽  
P. C. Magherini ◽  
D. Manzoni ◽  
O. Pompeiano

1. The electrical activity of 106 individual neurons located in the precerebellar lateral reticular nucleus (NRL) and the surrounding medullary reticular formation (RF) has been recorded in precollicular decerebrate cats during sinusoidal tilt around the longitudinal axis of the whole animal leading to stimulation of labyrinth receptors. 2. Among these lateral reticular neurons tested, 48 of 712 (67.6%) NRL neurons and 11 of 35 (31.4%) RF neurons responded to slow rotation of the animal at the standard frequency of 0.026 Hz and at the peak amplitude of displacement of 5-10 degrees. 3. All the responsive units showed a periodic modulation of firing rate during the sinusoidal stimulus. In particular, 35 of 57 units (i.e., 61.4%) were excited during side-up and depressed during side-down tilt of the whole animal; on the other hand, 14 of 57 units (i.e., 24.6%) showed the opposite behavior. In both instances, the peak of the responses occurred with an average phase lead of about 16 degrees with respect to the extreme side-up or side-down position of the animal. The remaining eight units (i.e., 14%) showed a phase shift of the peak of their response of about 90 degrees with respect to the animal position. 4. The sensitivity of the responses, expressed in percentage change of the average firing rate per degree of displacement, did not change by increasing the peak amplitude of tilt from 5 to 15 degrees at the frequency of 0.026 Hz. This finding indicates that the system was relatively linear with respect to the amplitude of stimulation. The sensitivity of the units, however, slightly increased but the phase angle of the responses did not change by increasing the frequency of tilting from 0.015 to 0.15 Hz at the peak amplitude of 5 or 10 degrees. These findings indicate that the responses depended on stimulation of macular labyrinth receptors. 5. Most of the lateral reticular units affected by tilt received also a bilateral convergent input from the hindlimbs. 6. These observations are related to the results of previous studies in which the responses of macular afferents, vestibular nuclei neurons, and corticocerebellar Purkinje (P) cells to sinusoidal tilt of the whole animal have been investigated. A possible role of lateral reticular neurons in the labyrinth control of posture in decerebrate cat is also discussed.


1992 ◽  
Vol 68 (2) ◽  
pp. 471-484 ◽  
Author(s):  
R. Boyle ◽  
J. M. Goldberg ◽  
S. M. Highstein

1. A previous study measured the relative contributions made by regularly and irregularly discharging afferents to the monosynaptic vestibular nerve (Vi) input of individual secondary neurons located in and around the superior vestibular nucleus of barbiturate-anesthetized squirrel monkeys. Here, the analysis is extended to more caudal regions of the vestibular nuclei, which are a major source of both vestibuloocular and vestibulospinal pathways. As in the previous study, antidromic stimulation techniques are used to classify secondary neurons as oculomotor or spinal projecting. In addition, spinal-projecting neurons are distinguished by their descending pathways, their termination levels in the spinal cord, and their collateral projections to the IIIrd nucleus. 2. Monosynaptic excitatory postsynaptic potentials (EPSPs) were recorded intracellularly from secondary neurons as shocks of increasing strength were applied to Vi. Shocks were normalized in terms of the threshold (T) required to evoke field potentials in the vestibular nuclei. As shown previously, the relative contribution of irregular afferents to the total monosynaptic Vi input of each secondary neuron can be expressed as a %I index, the ratio (x100) of the relative sizes of the EPSPs evoked by shocks of 4 x T and 16 x T. 3. Antidromic stimulation was used to type secondary neurons as 1) medial vestibulospinal tract (MVST) cells projecting to spinal segments C1 or C6; 2) lateral vestibulospinal tract (LVST) cells projecting to C1, C6; or L1; 3) vestibulooculo-collic (VOC) cells projecting both to the IIIrd nucleus and by way of the MVST to C1 or C6; and 4) vestibuloocular (VOR) neurons projecting to the IIIrd nucleus but not to the spinal cord. Most of the neurons were located in the lateral vestibular nucleus (LV), including its dorsal (dLV) and ventral (vLV) divisions, and adjacent parts of the medial (MV) and descending nuclei (DV). Cells receiving quite different proportions of their direct inputs from regular and irregular afferents were intermingled in all regions explored. 4. LVST neurons are restricted to LV and DV and show a somatotopic organization. Those destined for the cervical and thoracic cord come from vLV, from a transition zone between vLV and DV, and to a lesser extent from dLV. Lumbar-projecting neurons are located more dorsally in dLV and more caudally in DV. MVST neurons reside in MV and in the vLV-DV transition zone.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 54 (4) ◽  
pp. 1006-1025 ◽  
Author(s):  
C. Xerri ◽  
S. Gianni ◽  
D. Manzoni ◽  
O. Pompeiano

The response characteristics of neurons located in the lateral vestibular nucleus (LVN) to neck rotation at 0.026 Hz, 10 degrees peak displacement, have been investigated in precollicular decerebrate cats submitted to ipsilateral acute (aVN) or chronic vestibular neurectomy (cVN). On the whole, 105 units were tested after aVN (i.e., during the first postoperative hours) and 132 units after cVN (i.e., after full compensation of the postural and locomotor deficits). The neurons were histologically located either in the rostroventral (rvLVN) or the dorsocaudal part (dcLVN) of Deiters' nucleus, which are known to project mainly to the cervical and the lumbosacral cord, respectively. Moreover, 55 units in the former group and 66 units in the latter group were identified as vestibulospinal neurons projecting to lumbosacral segments of the spinal cord. The responses of these 237 LVN neurons to the neck input were then compared with those of 120 LVN neurons recorded previously in decerebrate cats with intact labyrinths. Whereas 58.3% of the LVN units recorded in control experiments were responsive to neck rotation, 69.5% of the units were affected by this stimulation at the acute stage of the neurectomy and 74.2% at the chronic stage. This increase in responsive units after aVN and cVN with respect to the controls was found exclusively in the dcLVN. The mean discharge rate of the responsive LVN neurons decreased from 40.7 +/- 48.9 (SD) imp/s in control experiments to 22.1 +/- 15.8 (SD) imp/s after a VN. Similar value was also obtained after cVN [25.0 +/- 17.2 (SD) imp/s], suggesting that compensation of the postural deficits elicited by the vestibular neurectomy results from a redistribution of the excitatory drive within different populations of LVN neurons. Indeed, the relation found in control experiments, i.e., that the faster the conduction velocity of vestibulospinal axons the lower was the unit discharge at rest, was lost after aVN, due to a decrease in resting discharge of the slow units. The mean discharge rate of the slow units, however, recovered after cVN, so that the negative correlation between resting discharge rate and axonal conduction velocity was reestablished. The average gain and sensitivity of the first harmonic response of the LVN neurons to neck rotation recorded after aVN and cVN were comparable to those obtained in preparations with the vestibular nerves intact.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (3) ◽  
pp. 1220-1226 ◽  
Author(s):  
D. Czepita ◽  
S. N. Reid ◽  
N. W. Daw

1. Cats were reared in the dark to 3, 5, and 11 mo. We studied the N-methyl-D-aspartate (NMDA) receptor contribution to the visual response in the cortex, defined as the percentage reduction in visual response after application of 2-amino-5-phosphonovaleric acid (APV). We also studied the firing rate in response to the optimal visual stimulus and the spontaneous activity. We made comparisons of all these properties between light-reared and dark-reared animals. 2. The NMDA receptor contribution to the visual response in layers IV, V, and VI of dark-reared animals was substantially above that in light-reared animals at all ages tested. 3. The specificity of receptive field properties in dark-reared animals showed some degeneration between 6 wk and 3 mo of age. At > or = 3 mo, almost no cells were specific for orientation and direction of movement. 4. Firing rate was lower in dark-reared animals at all ages, suggesting a decrease in excitatory drive to the visual cortex. 5. Spontaneous activity was equal in dark- and light-reared animals, suggesting that the overall level of activity (including visual responses as well as spontaneous activity) in light-reared animals is higher than in dark-reared animals. This should tend to upregulate glutamate receptors in general in dark-reared animals.


2018 ◽  
Vol 119 (1) ◽  
pp. 73-83 ◽  
Author(s):  
Shawn D. Newlands ◽  
Ben Abbatematteo ◽  
Min Wei ◽  
Laurel H. Carney ◽  
Hongge Luan

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.


1987 ◽  
Vol 58 (4) ◽  
pp. 719-738 ◽  
Author(s):  
S. M. Highstein ◽  
J. M. Goldberg ◽  
A. K. Moschovakis ◽  
C. Fernandez

1. Intracellular recordings were made from secondary neurons in the vestibular nuclei of barbiturate-anesthetized squirrel monkeys. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by stimulation of the ipsilateral vestibular nerve (Vi) were measured. An electrophysiological paradigm, described in the preceding paper (26), was used to determine the proportion of irregularly (I) and regularly (R) discharging Vi afferents making direct connections with individual secondary neurons. The results were expressed as a % I index, an estimate for each neuron of the percentage of the total Vi monosynaptic input that was derived from I afferents. The secondary neurons were also classified as I, R, or M cells, depending on whether they received their direct Vi inputs predominantly from I or R afferents or else from a mixture (M) of both kinds of Vi fibers. The neurons were located in the superior vestibular nucleus (SVN) or in the rostral parts of the medical or lateral (LVN) vestibular nuclei. 2. Antidromic activation or reconstruction of axonal trajectories after intrasomatic injection of horseradish peroxidase (HRP) was used to identify three classes of secondary neurons in terms of their output pathways: 1) cerebellar-projecting (Fl) cells innervating the flocculus (n = 26); 2) rostrally projecting (Oc) cells whose axons ascended toward the oculomotor (IIIrd) nucleus (n = 27); and 3) caudally projecting (Sp) cells with axons descending toward the spinal cord (n = 13). Two additional neurons, out of 21 tested, could be antidromically activated both from the level of the IIIrd nucleus and from the spinal cord. 3. The Vi inputs to the various classes of relay neurons differed. As a class, Oc neurons received the most regular inputs. Sp neurons had more irregular inputs. Fl neurons were heterogeneous with similar numbers of R, M, and I neurons. The mean values (+/- SD) of the % I index for the Oc, Fl, and Sp neurons were 34.7 +/- 24.7, 51.9 +/- 30.4, and 61.8 +/- 18.0%, respectively. Only the Oc neurons had a % I index that was similar to the proportion of I afferents (34%) in the vestibular nerve (cf. Ref. 26). 4. The commissural inputs from the contralateral vestibular nerve (Vc) also differed for the three projection classes. Commissural inhibition was most common in Fl cells: 22/25 (88%) of the neurons had Vc inhibitory postsynaptic potentials (IPSPs) and 1/25 (4%) had a Vc EPSP. In contrast, Vc inputs were only observed in approximately half the Oc and Sp neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


2002 ◽  
Vol 88 (4) ◽  
pp. 2104-2113 ◽  
Author(s):  
Sam Musallam ◽  
R. D. Tomlinson

Angular and translational accelerations excite the semicircular canals and otolith organs, respectively. While canal afferents approximately encode head angular velocity due to the biomechanical integration performed by the canals, otolith signals have been found to approximate head translational acceleration. Because central vestibular pathways require velocity and position signals for their operation, the question has been raised as to how the integration of the otolith signals is accomplished. We recorded responses from 62 vestibular-only neurons in the vestibular nucleus of two monkeys to position transients in the naso-occipital and interaural orientations and varying directions in between. Responses to the transients were directionally asymmetric; one direction elicited a response that approximated the integral of the acceleration of the stimulus. In the opposite direction, the cells simply encoded the acceleration of the motion. We present a model that suggests that a neural integrator is not needed. Instead a neuron with a long membrane time constant and an excitatory postsynaptic potential duration that increases with the firing rate of the presynaptic cell can emulate the observed behavior.


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