Vestibular compensation in lampreys: restoration of symmetry in reticulospinal commands
1 The Nobel Institute for Neurophysiology, Department of Neuroscience,
Karolinska Institute, SE-171 77, Stockholm, Sweden
2 A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State
University, Moscow 119899, Russia
* Author for correspondence (e-mail: Tatiana.Deliagina{at}neuro.ki.se)
Accepted 14 October 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: postural control, locomotion, vestibular compensation, reticulospinal system, lamprey, Lampetra fluviatilis
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We use a simple biological model the lamprey, a lower vertebrate
(cyclostome), for studying the effect of UL on postural stability, as well as
the process of recovery of postural function. The basic design of the lamprey
CNS, and especially of the brain stem and spinal cord, is similar to that of
higher vertebrates (Nieuwenhuys et al.,
1998), but the lamprey presents many more opportunities for
analytical studies of the nervous mechanisms for postural control, including
studies at the network and cellular levels
(Orlovsky, 1991
;
Macpherson et al., 1997
).
A swimming lamprey actively stabilizes the dorsal-side-up orientation of
its body by the activity of the postural control system driven by vestibular
input (de Burlet and Versteegh,
1930; Ullén et al.,
1995a
; Deliagina,
1995
,
1997a
,b
).
Visual input plays only a modulatory role: a unilateral eye illumination
evokes a roll tilt towards the source of light the `dorsal light
response' (Ullén et al.,
1993
,
1995b
), first described in
bony fishes by von Holst
(1935
).
Because the postural control system in the lamprey is driven primarily by
vestibular input, the effect of UL in this animal is most dramatic. After UL,
lampreys with intact eyes completely lose equilibrium and during swimming
continuously roll toward the damaged labyrinth
(de Burlet and Versteegh, 1930;
Deliagina, 1995
,
1997a
). During this period,
however, the equilibrium can be temporarily restored by creating an asymmetry
in visual input, that is, by illuminating the eye contralateral to UL, or by
electrically stimulating the corresponding optic nerve. During the process of
vestibular compensation, which lasts a few weeks, the UL animals gradually
recover their capacity to maintain equilibrium (Deliagina,
1995
,
1997a
).
The postural network in the lamprey has been characterized in considerable
detail. Important elements of this network are the reticulospinal (RS) neurons
(Nieuwenhuys, 1972), which
transmit commands for postural corrections from the brainstem to the spinal
cord. The RS neurons receive vestibular input through interneurons of the
vestibular nuclei (Koyama et al.,
1989
; Northcutt,
1979
; Rovainen,
1979
; Rubinson,
1974
; Stefanelli and Caravita,
1970
; Tretjakoff,
1909
). They also receive inputs from other sensory systems as well
as from the forebrain, brainstem centers and spinal cord
(Deliagina et al., 1993
;
Viana Di Prisco et al., 1995
;
Dubuc et al., 1993
; Rovainen,
1967
,
1979
;
Wickelgren, 1977
). In the
spinal cord, the RS neurons affect motoneurons and different classes of
interneurons (Brodin et al.,
1988
; Ohta and Grillner,
1989
; Rovainen,
1967
,
1974
,
1979
;
Wannier et al., 1995
; Zelenin
et al., 2001
,
2003
).
Responses of larger RS neurons to natural vestibular stimulation (roll
tilts) and eye illumination were initially investigated in vitro
(Deliagina et al., 1992a;
Orlovsky et al., 1992
;
Deliagina et al., 1993
;
Ullén et al., 1996
),
and recently in vivo (Deliagina
and Fagerstedt, 2000
). These experiments have shown that the
majority of RS neurons were activated by contralateral roll tilt; this
activation was mainly due to excitatory input from specific groups of
contralateral vestibular afferents
(Deliagina et al., 1992b
). A
unilateral visual input evoked excitation of the ipsilateral RS neurons and
inhibition of the contralateral ones.
Subsequent studies (Deliagina and
Pavlova, 2002) have shown that UL caused a dramatic asymmetry in
the responses of RS neurons to roll tilts: the responses persisted in the
ipsilateral RS neurons and disappeared in the contralateral ones. It was also
found that illumination of the eye contralateral to the UL resulted in a
restoration of symmetry in the bilateral activity of the RS system. Since
illumination of this eye also leads to a restoration of equilibrium in
non-compensated UL lampreys (Deliagina,
1997b
), it was suggested that the loss of equilibrium and
continuous rolling in UL lampreys is caused by the asymmetry in descending RS
commands, and a recovery of postural control occurs as a result of restoration
of symmetry in these commands (Deliagina,
1997b
; Deliagina and Pavlova,
2002
).
The goal of the present study was to test this hypothesis. For this
purpose, by means of chronically implanted electrodes, we recorded responses
to roll tilts in the left and right RS neurons in fully compensated animals.
These data were compared to the control data, that is, to the vestibular
responses recorded in non-compensated animals soon after UL
(Deliagina and Pavlova, 2002).
These experiments have shown that the ability of lampreys to maintain
equilibrium is associated with the presence of vestibular responses in RS
neurons on the side contralateral to the UL. These results support the
hypothesis that a recovery of postural control impaired by UL is the result of
restoration of symmetry in the supraspinal motor commands.
A brief account of this study has been published as an abstract
(Pavlova and Deliagina,
2002b).
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Electrodes
The activity of RS neurons was recorded from their axons in the spinal cord
by means of chronically implanted macroelectrodes as described in detail in
previous reports (Deliagina et al.,
2000; Deliagina and Fagerstedt,
2000
). In short, the electrodes (silver wires 75 µm in diameter
and 3 mm in length) were oriented in parallel to the long spinal axons. They
allowed an almost exclusive recording of the spike activity from larger fibres
that have a conduction velocity of more than 2 m s1. In the
lamprey, such a high conduction velocity is a characteristic of larger RS
neurons (Rovainen, 1967
,
1979
). The electrodes were
glued to a plastic plate (4 mm long, 2 mm wide and 0.25 mm thick). Two
different designs of the electrode array were used, one with two electrodes
and the other with four electrodes (Fig.
1A).
|
Surgery
Animals were operated on twice under MS-222 (Sigma-Aldrich, Stockholm,
Sweden) anesthesia (100 mg l1). During the first surgery,
the UL was performed. Sixty days after UL, when all animals reached a
compensated state (that is they swam without rotation; see
Deliagina, 1997a), the second
surgery was performed and the recording electrodes were implanted.
The UL was performed either on the left side (N=3) or on the right
side (N=3) using the technique described in detail previously
(Deliagina, 1995,
1997a
). In short, a hole was
made in the dorsolateral aspect of the vestibular capsule and the labyrinth
was removed with a pair of fine forceps under visual control. After removal,
the intact medial wall of the vestibular capsule and a stump of the eighth
nerve could be seen. Post mortem investigation showed that, in all
cases, removal of the vestibular organ was complete and the medial wall of the
capsule was undamaged.
The implantation of electrodes was performed as described in detail by
Deliagina et al. (2000) and by
Deliagina and Fagerstedt
(2000
). Two plates with
electrodes were implanted at different rostrocaudal levels. The plate with two
electrodes was implanted at the level of the third gill, and the plate with
four electrodes 2030 mm more caudally. The electrodes were facing the
dorsal aspect of the spinal cord, as shown schematically in
Fig. 1A.
Vestibular stimulation
Vestibular responses of RS neurons were recorded 1 or 2 days after
implantation of the electrodes. The arrangements for vestibular stimulation,
as well as the characteristics of stimuli, were described previously
(Deliagina and Fagerstedt,
2000). In short, the lamprey was positioned in the tube and
rotated about the longitudinal body axis
(Fig. 1B). To reveal the
dynamic characteristics of vestibular responses, they were rotated in 45°
steps. To reveal a directional sensitivity of neurons, two full turns were
produced in opposite directions (Fig.
1C, bottom). To examine the effect of tonic visual input on
vestibular responses, the responses were examined both in light and in
darkness. Testing in light was performed in an aquarium that was illuminated
by a 100 W white incandescent lamp mounted above the aquarium at a distance of
2 m. A considerable part of the light was reflected from a sheet of white
paper positioned under the transparent bottom of the aquarium, thus producing
a rather diffuse illumination within the aquarium.
Data processing
Signals from the electrodes were amplified by conventional AC amplifiers,
digitized with a sampling frequency of 10 kHz and stored on the hard disk of
an IBM AT compatible computer by means of data acquisition software (Digitdata
1200/Axoscope, Axon Instruments, Inc., Union City, CA, USA). The recorded
multiunit spike trains were separated into unitary waveforms, representing the
activity of individual axons, by means of data analysis software (`Spike
sorting', Datapac III, Run Technologies, Inc., Laguna Hills, CA, USA). The
analysis was based on the selection of distinguishable unitary waveforms
occurring on one electrode, or occurring simultaneously on two or more
electrodes of the array; this technique was previously described in detail
(Deliagina and Fagerstedt,
2000; Deliagina and Pavlova,
2002
; Pavlova and Deliagina,
2002a
,
2003
).
To determine the angular zones of sensitivity of individual RS neurons, their vestibular responses were characterized quantitatively. For this purpose, each step of rotation was divided into three intervals (13, see inset in Fig. 1C), and the firing frequency of a neuron was measured separately for each interval in each step. The activity in interval 1 (during movement) will be termed `dynamic response'; the activity in intervals 2 and 3 (when a new position was maintained) will be termed `early' and `late static responses', respectively.
The mediolateral position of individual axons in the spinal cord was
estimated by comparing the amplitudes of the same spike recorded by different
electrodes of the same array. The conduction velocity in individual axons
could also be measured using the time delay between spikes from the same axon
recorded by the rostral and caudal electrodes
(Deliagina and Fagerstedt,
2000).
All analytical procedures and possible sources of errors during the spike
sorting have also been fully described in recent reports
(Deliagina and Fagerstedt,
2000; Deliagina and Pavlova,
2002
; Pavlova and Deliagina,
2002a
,
2003
).
All quantitative data in this study are presented as the mean ± S.E.M. Paired Student's t-tests were used to determine the statistical significance when comparing different means; the confidence level was set at P=0.05. All statements in the following text about the similarity or difference between the neuronal responses are based on these statistical criteria.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Vestibular responses of RS neurons in light
The activity in RS pathways in light was recorded in all six compensated UL
animals. Normally, the resting activity in RS neurons was low or absent, and
vestibular stimulation activated the neurons. This is illustrated in
Fig. 1C for the animal that was
fully compensated after the left UL. Traces E1 and E2 show the mass activity
in RS pathways recorded by the left and right electrodes of the rostral array,
respectively (electrodes 1 and 2 in Fig.
1A). Using the spike-sorting program, the activity of seven
individual axons was separated from the mass activity. All three neurons with
their axons located on the left side of the spinal cord, that is, ipsilateral
to the UL (L1L3, the i-UL group) had very similar patterns of
responses. In the first turn (rotation toward the UL) they exhibited almost no
activity. In the second turn (rotation toward the intact, contralateral
labyrinth), the neurons exhibited a dynamic response with any change of
position. In addition, they had static responses within the zone 45°R to
135°R.
The neurons with their axons located on the right side of the spinal cord (R1R4, the co-UL group) exhibited more diverse patterns of responses. The neurons R1 and R2 responded statically at the positions when the UL side was facing downward, either in the first turn (R1) or in both turns (R2). The neurons R3 and R4 responded dynamically to any change of position in the first turn, whereas their static responses were weak (in R3) or absent (in R4).
Altogether, 64 RS neurons were recorded in six animals in the light. The
overwhelming majority of them (61 neurons, or 95%) exhibited specific
responses to vestibular stimulation: they were activated more strongly by
rotation towards the contralateral labyrinth than in the opposite direction
and/or they had specific angular zones of responses. A small proportion of
neurons (3 units, or 5%), were activated by tilts in any direction, and their
activity did not correlate with any particular spatial orientation. In intact
animals, such neurons were also rarely observed
(Deliagina and Fagerstedt,
2000). Of the 61 neurons with specific vestibular responses, 31
neurons were located on the side ipsilateral to the UL (the i-UL group) and 30
neurons on the opposite side (the co-UL group).
To describe qualitatively the vestibular responses in the i-UL and co-UL
neuron groups, two characteristics were used
(Deliagina and Fagerstedt,
2000; Deliagina and Pavlova,
2002
; Pavlova and Deliagina,
2002a
,
2003
): (1) the number of
simultaneously active neurons, and (2) the mean discharge frequency of these
neurons. The number of active neurons was calculated separately for each
animal and then averaged over all six animals.
Fig. 2Ai shows a histogram of the number of simultaneously active i-UL neurons. Along the horizontal axis, the successive angles of roll tilt during two turns (a and b) performed in opposite directions are indicated. To combine the data obtained with the left and right UL, turn a represents the responses obtained with rotation toward the intact labyrinth, and turn b, toward the UL. One can see that during turn a any change of orientation evoked dynamic responses in most neurons. During turn b, the dynamic responses were much weaker than in turn a. Static responses were also more pronounced in turn a, at the positions 45°co to 135°co. When the same positions were reached by rotation in the opposite direction (turn b), only a small proportion of neurons were statically activated.
|
To evaluate the directional sensitivity of i-UL neurons, for each of the animals we calculated the mean number of neurons responding dynamically to sequential steps in turn a, and then averaged this value over all six animals; similar calculations were performed for turn b. The mean value of response in turn a was 3.6±0.1 neurons versus 0.8±0.1 neurons in turn b. The difference was statistically significant.
Fig. 2Bi shows the frequency curve for the i-UL group of RS neurons. One can see that the neurons were active mostly in turn a. In this turn, the dynamic responses were much stronger than the static ones. The mean value of the dynamic responses in turn a was 3.3±0.4 Hz versus 0.4±0.1 Hz in turn b. This difference was also statistically significant.
Thus, according to both characteristics (the number of active neurons and
their frequencies), the principal feature of the i-UL neurons is their much
stronger responses in turn a as compared to turn b. In this respect, the
responses were similar to those of RS neurons in intact lampreys observed in
the previous studies (Deliagina and
Fagerstedt, 2000; Deliagina and
Pavlova, 2002
).
As shown previously (Deliagina and
Pavlova, 2002), the main effect of UL in the non-compensated
animals was the lack of activity (absence of vestibular responses) in co-UL
neurons (see figs 5B2 and 6B2 in Deliagina
and Pavlova, 2002
). In contrast, the present study showed that
this population in the compensated animals was active. In six animals, we
recorded 30 co-UL neurons responding to vestibular stimulation. This number
was almost equal to the number of i-UL neurons (N=31) recorded by the
same electrodes. Fig. 2Aii
shows a histogram of the number of simultaneously active co-UL neurons, and
Fig. 2Bii, a histogram of their
frequencies. Turn a is the responses obtained with rotation toward the UL, and
turn b with rotation toward the intact labyrinth. Both histograms were
qualitatively similar to those for i-UL neurons
(Fig. 2Ai,Bi), that is, the
responses in turn a were larger than the responses in turn b. For the number
of active neurons, the mean value of responses in turn a was 2.6±0.4
neurons versus 1.4±0.2 neurons in turn b. For the frequency
curve, the mean value of responses in turn a was 2.2±0.3 Hz
versus 0.9±0.1 Hz in turn b. The difference in both cases was
statistically significant. However, the response magnitude in turn a in the
co-UL group was slightly smaller than in the i-UL group (compare
Fig. 2Bii,Bi). The mean value
of responses in the co-UL group was 2.2±0.3 Hz versus 3.3±0.4 Hz
in the i-UL group. The difference was statistically significant.
Vestibular responses of RS neurons in darkness
To characterize the significance of visual input for the generation of
vestibular responses in the compensated animals, three animals (out of six
animals tested in light, see above) were also tested in darkness. The main
result of these tests was that vestibular responses on both sides persisted in
darkness. In the i-UL group, the responses in darkness
(Fig. 3Ai,Bi) were very similar
to those in light (Fig.
2Ai,Bi). In the co-UL group, the response pattern in darkness
(Fig. 3Aii,Bii) was also
similar to that in light (Fig.
2Aii,Bii). However, a total number of responding i-UL and co-UL
neurons in the three animals tested in darkness (N=14 and 12,
respectively) was smaller than in the same animals tested in light
(N=21 and 18, respectively). The difference was statistically
significant.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The key elements of the postural system in the lamprey are the left and
right groups of reticulospinal (RS) neurons, transmitting commands for
postural corrections to the spinal cord
(Deliagina et al., 2002).
Recently it was found that UL causes a dramatic asymmetry in these commands:
the vestibular-evoked activity on the lesioned side persisted after UL,
whereas the activity on the opposite side disappeared completely
(Deliagina and Pavlova, 2002
).
It was also found that illumination of the eye contralateral to the UL results
in a restoration of symmetry in the bilateral activity of RS system. Since
illumination of this eye also leads to a restoration of equilibrium in
swimming, non-compensated lampreys
(Deliagina, 1997b
), it was
suggested that the loss of equilibrium in UL lampreys is caused by the
asymmetry in the descending RS commands, and a recovery of postural control
during a process of vestibular compensation is the result of a restoration of
symmetry in these commands.
The main result of the present study is that vestibular responses in RS
neurons on the side contralateral to the UL (the co-UL group), which were
absent when tested in the non-compensated animals a few days after UL
(Deliagina and Pavlova, 2002),
were present in the compensated animals
(Fig. 2Aii,Bii). This finding
strongly supports the hypothesis that a restoration of bilateral symmetry in
the RS commands underlies a recovery of equilibrium control.
However, the restored vestibular responses in the co-UL neurons
(Fig. 2Aii,Bii) differed, to
some extent, from the normal ones in intact animals
(Deliagina and Pavlova, 2002),
or from the responses in the i-UL group with the main (contralateral)
vestibular input intact (Fig.
2Ai,2Bi). First, the magnitude of the restored responses was
reduced by 3040%. Second, the co-UL group was less homogenous than the
i-UL group: in addition to the neurons responding mainly in the turn towards
the UL, some neurons responded in both turns
(Fig. 1C).
In behavioral experiments it was found that the process of vestibular
compensation in lampreys strongly depends on the presence of visual input.
Upon reaching a compensated state, however, this input becomes nonessential
for the maintenance of equilibrium, and the eyes can even be removed
(Deliagina,
1997a,b
).
It was suggested that in the compensated animals the restored activity in the
co-UL neurons does not require any significant support from the visual input.
This hypothesis was confirmed in the present study; we found that vestibular
responses in the co-UL neurons that were observed in light
(Fig. 2Aii,Bii), persisted also
in darkness (Fig. 3Aii,Bii),
though their magnitude was slightly reduced. These data also support a more
general assumption that restoration of the `central symmetry' (i.e. the
symmetry in the activity of vestibular nuclei and their targets) constitutes
an essential component of vestibular compensation
(Deliagina et al., 1997
; for a
review, see Curthoys and Halmaguyi,
1999
).
A possible functional role of the restored activity in the co-UL neurons
can be considered in the framework of the conceptual model of the roll control
system proposed earlier (Deliagina,
1997a; Deliagina and Pavlova,
2002
; Zelenin et al.,
2000
) (Fig. 4A).
The key elements of the model are the left and right groups of RS neurons,
RS(L) and RS(R). The main input to these neurons is from the contralateral
labyrinth, whereas the input from the ipsilateral labyrinth is much weaker.
Each input contains both excitatory and inhibitory components; the components
depend differently on the tilt angle
(Deliagina and Pavlova, 2000
).
Owing to these inputs, the activity of RS neurons is orientation dependent,
with its peak at
90° of contralateral roll tilt
(Fig. 4B). The two groups of
neurons also receive an excitatory input from the ipsilateral eye and an
inhibitory input from the contralateral eye. It was suggested that each of the
groups, via spinal mechanisms, elicits ipsilateral rotation of the animal
(black and white arrows in Fig.
4A,B). The system will stabilize the orientation in space with
equal effects produced by RS(L) and RS(R), that is, the dorsal-side-up
position (equilibrium point in Fig.
4B).
|
The model explains the loss of equilibrium after UL in the following way.
As a result of the loss of the main vestibular input from the contralateral
labyrinth, the UL causes inactivation of RS neurons on the contralateral side
(Deliagina and Pavlova, 2002),
as illustrated for the right-side labyrinthectomy in
Fig. 4C. Because of the
inactivation of RS(L), the two activity curves no longer intersect, the system
has no equilibrium point, and the dominating RS(R) causes the main postural
deficit: rolling of the lamprey to the right.
The model implies that restoration of postural equilibrium during
vestibular compensation is due to a recovery of activity in the co-UL group of
RS neurons, so that this group of neurons can counteract the i-UL group, and
the two activity curves will intersect again
(Fig. 4D). The present study
has shown that the vestibular-induced activity indeed re-appeared in the co-UL
neurons (Fig. 2Aii,Bii and
Fig. 3Aii,Bii). The angle at
which the RS(L) and RS(R) curves will intersect depends on the degree of
restoration of the activity (vestibular responses) in the deafferented RS
neurons. If these responses are weaker than those in the i-UL neurons, the
equilibrium point will be shifted toward the UL (as in
Fig. 4D), and the roll control
system will stabilize this tilted position the behavior often observed
in the compensated animals (Deliagina,
1997a).
Presumed cellular and network mechanisms underlying the recovery of central
symmetry after UL in amphibians and mammals have been discussed by a number of
authors (Darlington and Smith,
1996; Ris et al.,
1995
,
2001
;
Vibert et al., 1999
;
Curthoys and Halmagyi, 1999
;
Smith and Curthoys, 1989
;
Dieringer, 1995
). Some of
these mechanisms can be considered in relation to the lamprey.
In previous studies it was shown that two inputs to RS neurons, from the
contralateral and ipsilateral labyrinths
(Fig. 4A), have similar spatial
zones of sensitivity and thus supplement each other when eliciting vestibular
responses in RS neurons. The ipsilateral input, however, is much weaker than
the contralateral one and, when acting alone, is not able to activate RS
neurons in the non-compensated animals
(Deliagina and Pavlova, 2002).
The present study has shown that recovery of equilibrium in UL animals is
accompanied by the appearance of responses of RS neurons to the signals coming
from the ipsilateral labyrinth. The appearance of responses to previously
sub-threshold signals can be explained by changes in the membrane properties
(excitability) of either RS neurons themselves, or pre-reticular neurons
transmitting vestibular signals, as well as by changes in synaptic efficacy of
the existing synapses and/or reactive synaptogenesis in the
vestibulo-reticular pathways. An increase of the tonic excitatory drive to RS
neurons from other sources can also contribute. These factors could explain
the appearance of responses within the angular zones similar to the normal
ones. However, an increased diversity of angular zones of restored responses
as compared to normal responses (Fig.
1C) suggests the appearance of new connections originating from
the vestibular afferents with corresponding characteristics of their spatial
sensitivity.
In conclusion, the present study has demonstrated that, in the lampreys subjected to ablation of one labyrinth, the recovery of an important motor function the maintenance of equilibrium is associated with a restoration of a close-to-normal pattern of supraspinal motor commands. The corresponding plastic changes in brainstem neuronal networks remain to be identified.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Brodin, L., Grillner, S., Dubuc, R., Ohta, Y., Kasicki, S. and Hökfelt, T. (1988). Reticulospinal neurons in lamprey: transmitters, synaptic interactions, and their role during locomotion. Arch. Ital. Biol. 126,317 -345.[Medline]
Curthoys, I. S. and Halmagyi, G. M. (1999). Vestibular compensation. Adv. Otolaringol. 55, 82-110.
Darlington, C. L. and Smith, P. F. (1996). The recovery of static vestibular function following peripheral vestibular lesions in mammals: the intrinsic mechanism hypothesis. J. Vestib. Res. 6,185 -201.[CrossRef][Medline]
de Burlet, H. M. and Versteegh, C. (1930). Ueber Bau und Funktion des Petromyzonlabyrinthes. Acta Oto-Laringol. Supplement 13,5 -58.
Deliagina, T. G. (1995). Vestibular compensation in the lamprey. NeuroRep. 6,2599 -2603.
Deliagina, T. G. (1997a). Vestibular
compensation in lampreys: impairment and recovery of equilibrium control
during locomotion. J. Exp. Biol.
200,1459
-1471.
Deliagina, T. G. (1997b). Vestibular
compensation in lampreys: role of vision at different stages of recovery of
equilibrium control. J. Exp. Biol.
200,2957
-2967.
Deliagina, T. G. and Fagerstedt, P. (2000).
Responses of reticulospinal neurons in intact lamprey to vestibular and visual
inputs. J. Neurophysiol.
83,864
-878.
Deliagina, T. G. and Pavlova, E. L. (2002).
Modifications of vestibular responses of individual reticulospinal neurons in
the lamprey caused by a unilateral labyrinthectomy. J.
Neurophysiol. 87,1
-14.
Deliagina, T. G., Orlovsky, G. N., Grillner, S. and Wallén, P. (1992a). Vestibular control of swimming in lamprey. 2. Characteristics of spatial sensitivity of reticulospinal neurons. Exp. Brain Res. 90,489 -498.[Medline]
Deliagina, T. G., Orlovsky, G. N., Grillner, S. and Wallén, P. (1992b). Vestibular control of swimming in lamprey. 3. Activity of vestibular afferents. Convergence of vestibular inputs on reticulospinal neurons. Exp. Brain Res. 90,499 -507.[Medline]
Deliagina, T. G., Grillner, S., Orlovsky, G. N. and Ullén, F. (1993). Visual input affects the response to roll in reticulospinal neurons of the lamprey. Exp. Brain Res. 95,421 -428.[Medline]
Deliagina, T. G., Popova, L. B. and Grant, G. (1997). The role of tonic vestibular input for postural control in rats. Arch. Ital. Biol. 135,239 -261.[Medline]
Deliagina, T. G., Zelenin, P. V., Fagerstedt, P., Grillner, S.
and Orlovsky, G. N. (2000). Activity of reticulospinal
neurons during locomotion in the freely behaving lamprey. J.
Neurophysiol. 83,853
-863.
Deliagina, T. G., Zelenin, P. V. and Orlovsky, G. N. (2002). Encoding and decoding of reticulospinal commands. Brain Res. Rev. 40,166 -177.[CrossRef][Medline]
Dieringer, N. (1995). `Vestibular compensation': Neural plasticity and its relations to functional recovery after labyrinthine lesions in frogs and other vertebrates. Prog. Neurobiol. 46,97 -129.[CrossRef][Medline]
Dubuc, R., Bongianni, F., Ohta, Y. and Grillner, S. (1993). Dorsal root and dorsal column mediated synaptic inputs to reticulospinal neurons in lampreys: involvement of glutamatergic, glycinergic, and GABAergic transmission. J. Comp. Neurol. 327,251 -259.[Medline]
Koyama, H., Kishida, R., Goris, R. C. and Kusunoki, T. (1989). Afferent and efferent projections of the VIIIth cranial nerve in the lamprey Lampetra japonica. J. Comp. Neurol. 280,663 -671.[Medline]
Macpherson, J., Deliagina, T. G. and Orlovsky, G. N. (1997). Control of body orientation and equilibrium in vertebrates. In Neurons, Networks and Motor Behavior (ed. P. S. G. Stein, S. Grillner, A. I. Selverston and D. Stuart), pp.257 -267. Cambridge, MA, USA: MIT Press.
Nieuwenhuys, R. (1972). Topological analysis of the brain stem of the lamprey Lampetra fluviatilis. J. Comp. Neurol. 145,165 -177.[Medline]
Nieuwenhuys, R., Donkelaarten, H. and Nicholson, C. (1998). The Central Nervous System of Vertebrates. Berlin: Springer.
Northcutt, R. G. (1979). Central projections of the eight cranial nerve in lampreys. Brain Res. 167,163 -167.[CrossRef][Medline]
Ohta, Y. and Grillner, S. (1989). Monosynaptic
excitatory amino acid transmission from the posterior rhombencephalic
reticular nucleus to spinal neurons involved in the control of locomotion in
lamprey. J. Neurophysiol.
62,1079
-1089.
Orlovsky, G. N. (1991). Gravistatic postural control in simpler systems. Curr. Opin. Neurobiol. 1, 612-627.
Orlovsky, G. N., Deliagina, T. G. and Wallén, P. (1992). Vestibular control of swimming in lamprey. 1. Responses of reticulospinal neurons to roll and pitch. Exp. Brain Res. 90,479 -488.[Medline]
Pavlova, E. L. and Deliagina, T. G. (2002a).
Responses of reticulospinal neurons in intact lamprey to pitch tilt.
J. Neurophysiol. 88,1136
-1146.
Pavlova, E. L. and Deliagina, T. G. (2002b). Modifications of vestibular responses in reticulospinal neurons underlying compensation of vestibular deficit in lamprey. Program no 168.1 2002 Abstract Viewer/itinerary planner. Washington, DC: Society for Neuroscience, Online.
Pavlova, E. L. and Deliagina, T. G. (2003).
Asymmetry in the pitch control system of the lamprey caused by a unilateral
labyrinthectomy. J. Neurophysiol.
89,2370
-2379.
Ris, L., de Waele, C., Serafin, M., Vidal, P.-P. and Godaux,
E. (1995). Neuronal activity in the ipsilateral vestibular
nucleus following unilateral labyrinthectomy in the alert guinea pig.
J. Neurophysiol. 74,2087
-2099.
Ris, L., Capron, B., Vibert, N., Vidal, P.-P. and Godaux, E. (2001). Modification of the pacemaker activity of vestibular neurons in brainstem slices during vestibular compensation in the guinea pig. Eur. J. Neurosci. 13,2234 -2240.[CrossRef][Medline]
Rovainen, C. M. (1967). Physiological and
anatomical studies on large neurons of central nervous system of the sea
lamprey (Petromyzon marinus). I. Müller and Mauthner cells.
J. Neurophysiol. 30,1000
-1023.
Rovainen, C. M. (1974). Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey. J. Comp. Neurol. 154,207 -223.[Medline]
Rovainen, C. M. (1979). Electrophysiology of
vestibulospinal and vestibuloreticulospinal systems in lampreys. J.
Neurophysiol. 42,745
-766.
Rubinson, K. (1974). The central distribution of VIII nerve afferents in larval Petromyzon marinus. Brain Behav. Evol. 10,121 -129.[CrossRef][Medline]
Schaefer, K. P. and Meyer, D. L. (1974). Compensation of vestibular lesions. In Handbook of Sensory Physiology. Vestibular System. Part 2: Psychophysics, Applied Aspects and General Interpretation Vol. 6/2 (ed. H. H. Kornhuber), pp.463 -490. Berlin: Springer.
Smith, P. F. and Curthoys, I. S. (1989). Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res. Rev. 14,155 -180.[Medline]
Stefanelli, A. and Caravita, S. (1970). Ultrastructural features of the synaptic complex of the vestibular nuclei of Lampetra planeri (Bloch). Z. Zellforsch. Mikrosk. Anat. 108,282 -296.[CrossRef][Medline]
Tretjakoff, D. (1909). Das nervensystem von Ammocoetes II. Gehirn. Arch. Mikrosk. Anat. Entwicklungsmech. 74,636 -779.
Ullén, F., Orlovsky, G. N., Deliagina, T. G. and Grillner, S. (1993). Role of dermal photoreceptors and lateral eyes in initiation and orientation of locomotion in lamprey. Behav. Brain Res. 54,107 -110.[CrossRef][Medline]
Ullén, F., Deliagina, T. G., Orlovsky, G. N. and
Grillner, S. (1995a). Spatial orientation of lamprey. 1.
Control of pitch and roll. J. Exp. Biol.
198,665
-673.
Ullén, F., Deliagina, T. G., Orlovsky, G. N. and
Grillner, S. (1995b). Spatial orientation of lamprey. 2.
Visual influence on orientation during locomotion and in the attached state.
J. Exp. Biol. 198,675
-681.
Ullén, F., Deliagina, T. G., Orlovsky, G. N. and Grillner, S. (1996). Visual potentiation of vestibular responses in lamprey reticulospinal neurons. Eur. J. Neurosci. 8,2298 -2307.[Medline]
Viana Di Prisco, G. V., Ohta, Y., Bongianni, F., Grillner, S. and Dubuc, R. (1995). Trigeminal inputs to reticulospinal neurons in lampreys are mediated by excitatory and inhibitory amino acids. Brain Res. 695,76 -80.[CrossRef][Medline]
Vibert, N., Babalian, A., Serafin, M., Gasc, J.-P., Muhlethaler, M. and Vidal, P.-P. (1999). Plastic changes underlying vestibular compensation in the guinea-pig persist in isolated, in vitro whole brain preparations. Neurosci. 93,413 -432.[CrossRef][Medline]
Vidal, P.-P., de Waele, C., Vibert, N. and Muhlethaler, M. (1998). Vestibular compensation revisited. Otolaringol. Head Neck Surg. 119, 34-42.
von Holst, E. (1935). Über den Lichtrückenreflex bei Fischen. Publ. Staz. Zool. Napoli 15,143 -158.
Wannier, T., Orlovsky, G. N. and Grillner, S. (1995). Reticulospinal neurones provide monosynaptic glycinergic inhibition of spinal neurones in lamprey. NeuroRep. 6,1597 -1600.
Wickelgren, W. O. (1977). Physiological and anatomical characteristics of reticulospinal neurones in lamprey. J. Physiol. 279,89 -114.
Zelenin, P. V., Deliagina, T. G., Grillner, S. and Orlovsky, G.
N. (2000). Postural control in the lamprey a study
with a neuro-mechanical model. J. Neurophysiol.
84,2880
-2887.
Zelenin, P. V., Grillner, S., Orlovsky, G. N. and Deliagina, T.
G. (2001). Heterogeneity of the population of command neurons
in the lamprey. J. Neurosci.
21,7793
-7803.
Zelenin, P. V., Pavlova, E. L., Grillner, S., Orlovsky, G. N.
and Deliagina, T. G. (2003). Comparison of the motor effects
of individual vestibulo- and reticulospinal neurons on dorsal and ventral
myotomes in lamprey. J. Neurophysol.
90,3161
-3167.