Responses of Reticulospinal Neurons in the Lamprey to Lateral Turns

2007 ◽  
Vol 97 (1) ◽  
pp. 512-521 ◽  
Author(s):  
A. Karayannidou ◽  
P. V. Zelenin ◽  
G. N. Orlovsky ◽  
T. G. Deliagina

When swimming, the lamprey maintains a definite orientation of its body in the vertical planes, in relation to the gravity vector, as the result of postural vestibular reflexes. Do the vestibular-driven mechanisms also play a role in the control of the direction of swimming in the horizontal (yaw) plane, in which the gravity cannot be used as a reference direction? In the present study, we addressed this question by recording responses to lateral turns in reticulospinal (RS) neurons mediating vestibulospinal reflexes. In intact lampreys, the activity of axons of RS neurons was recorded in the spinal cord by implanted electrodes. Vestibular stimulation was performed by periodical turns of the animal in the yaw plane (60° peak to peak). It was found that the majority of responding RS neurons were activated by the contralateral turn. By removing one labyrinth, we found that yaw responses in RS neurons were driven mainly by input from the contralateral labyrinth. We suggest that these neurons, when activated by the contralateral turn, will elicit the ipsilateral turn and thus will compensate for perturbations of the rectilinear swimming caused by external factors. It is also known that unilateral eye illumination elicits a contralateral turn in the yaw plane (negative phototaxis). We found that a portion of RS neurons were activated by the contralateral eye illumination. By eliciting an ipsilateral turn, these neurons could mediate the negative phototaxis.

2011 ◽  
Vol 105 (3) ◽  
pp. 1361-1371 ◽  
Author(s):  
P. V. Zelenin

Most vertebrates are capable of two forms of locomotion, forward and backward, strongly differing in the patterns of motor coordination. Basic mechanisms generating these patterns are located in the spinal cord; they are activated and regulated by supraspinal commands. In the lamprey, these commands are transmitted by reticulospinal (RS) neurons. The aim of this study was to reveal groups of RS neurons controlling different aspects of forward (FS) and backward (BS) swimming in the lamprey. Activity of individual larger RS neurons in intact lampreys was recorded during FS and BS by chronically implanted electrodes. It was found that among the neurons activated during locomotion, 27% were active only during FS, 3% only during BS, and 70% during both FS and BS. In a portion of RS neurons, their mean firing frequency was correlated with frequency of body undulations during FS (8%), during BS (34%), or during both FS and BS (22%), suggesting their involvement in control of locomotion intensity. RS activity was phasically modulated by the locomotor rhythm during FS (20% of neurons), during BS (29%), or during both FS and BS (16%). The majority of RS neurons responding to vestibular stimulation (and presumably involved in control of body orientation) were active mainly during FS. This explains the absence of stabilization of the body orientation observed during BS. We discuss possible functions of different groups of RS neurons, i.e., activation of the spinal locomotor CPG, inversion of the direction of propagation of locomotor waves, and postural control.


2000 ◽  
Vol 83 (2) ◽  
pp. 864-878 ◽  
Author(s):  
T. G. Deliagina ◽  
P. Fagerstedt

A lamprey maintains the dorsal-side-up orientation due to the activity of postural control system driven by vestibular input. Visual input can affect the body orientation: illumination of one eye evokes ipsilateral roll tilt. An important element of the postural network is the reticulospinal (RS) neurons transmitting commands from the brain stem to the spinal cord. Here we describe responses to vestibular and visual stimuli in RS neurons of the intact lamprey. We recorded activity from the axons of larger RS neurons with six extracellular electrodes chronically implanted on the surface of the spinal cord. From these multielectrode recordings of mass activity, discharges in individual axons were extracted by means of a spike-sorting program, and the axon position in the spinal cord and its conduction velocity were determined. Vestibular stimulation was performed by rotating the animal around its longitudinal axis in steps of 45° through 360°. Nonpatterned visual stimulation was performed by unilateral eye illumination. All RS neurons were classified into two groups depending on their pattern of response to vestibular and visual stimuli; the groups also differed in the axon position in the spinal cord and its conduction velocity. Each group consisted of two symmetrical, left and right, subgroups. In group 1neurons, rotation of the animal evoked both dynamic and static responses; these responses were much larger when rotation was directed toward the contralateral labyrinth, and the dynamic responses to stepwise rotation occurred at any initial orientation of the animal, but they were more pronounced within the angular zone of 0–135°. The zone of static responses approximately coincided with the zone of pronounced dynamic responses. The group 1 neurons received excitatory input from the ipsilateral eye and inhibitory input from the contralateral eye. When vestibular stimulation was combined with illumination of the ipsilateral eye, both dynamic and static vestibular responses were augmented. Contralateral eye illumination caused a decrease of both types of responses. Group 2neurons responded dynamically to rotation in both directions throughout 360°. They received excitatory inputs from both eyes. Axons of the group 2 neurons had higher conduction velocity and were located more medially in the spinal cord as compared with the group 1 neurons. We suggest that the reticulospinal neurons of group 1 constitute an essential part of the postural network in the lamprey. They transmit orientation-dependent command signals to the spinal cord causing postural corrections. The role of these neurons is discussed in relation to the model of the roll control system formulated in our previous studies.


1995 ◽  
Vol 198 (3) ◽  
pp. 675-681
Author(s):  
F Ullén ◽  
T G Deliagina ◽  
G N Orlovsky ◽  
S Grillner

The responses of attached lampreys to homogeneous visual stimulation and the role of visual stimuli in orientation during locomotion were investigated. Experiments were performed by video recording the responses of intact and lesioned animals to illumination. The following results were obtained. 1. In lampreys attached with their sucker mouth to the bottom of the aquarium, illumination of one eye evoked several possible motor responses (ordered after mean latency): (a) movement of the illuminated eye downwards, and the contralateral eye upwards; (b) rotation of the body around the longitudinal axis, with the illuminated side tilting downwards; (c) deviation of the caudal part of the anterior dorsal fin in the contralateral direction (away from the light); and (d) flexion of the neck and body towards the side of illumination. 2. Illumination of one eye in attached lampreys often resulted in detachment and subsequent movement in a direction away from the light source (negative phototaxis). This response was not related to the degree of roll tilt before detachment, so the negative phototaxis does not appear to be a consequence of the vestibular stimulation. 3. Negative phototaxis was also seen during locomotion: lampreys turned through 180 ° when they approached a brightly illuminated area. Photostimulation also affected their orientation in the transverse plane during swimming. Illumination of one eye from the side induced a roll movement, so that the illuminated side tilted downwards and the dorsum of the lamprey became turned towards the light. This is similar to the 'dorsal light response' of fish and shows that vision also plays a role in postural control in lampreys. 4. The behaviour of blinded animals differed strikingly from that of intact ones. Whereas intact animals preferentially swam close to the bottom, along horizontal trajectories, blinded animals showed episodes of continuous swimming upwards, near the water surface. During horizontal swimming, their orientation in the transverse plane remained normal, with the dorsal side up.


2002 ◽  
Vol 88 (3) ◽  
pp. 1136-1146 ◽  
Author(s):  
E. L. Pavlova ◽  
T. G. Deliagina

In the swimming lamprey, a postural control system maintains a definite orientation of the animal's longitudinal axis in relation to the horizon (pitch angle). Operation of this system is based on vestibular reflexes. Important elements of the postural network are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections from the brain stem to the spinal cord. Here we describe responses to vestibular stimulation (rotation of the animal in the pitch plane) in RS neurons of intact lampreys. The activity of neurons was recorded from their axons in the spinal cord by chronically implanted arrays of macroelectrodes. From the multielectrode recordings of mass activity, discharges in individual axons were extracted by means of a spike-sorting program, and the axon position in the spinal cord and its conduction velocity were determined. Vestibular stimulation was performed by rotating the animal in steps of 45° throughout 360° or by periodical “trapezoid” tilts between the nose-up and -down positions. Typically, the RS neurons exhibited both dynamic responses (activity during movement) and static responses (activity in a new sustained position). The neurons were classified into two groups according to their pattern of response. Group up neurons responded preferentially to nose-up rotation with maximal activity at 0–135° up. Group down neurons responded preferentially to nose-down rotation with maximal activity at 0–135° down. Neurons of the two groups also differed in the position of their axons in the spinal cord and axonal conduction velocity. An increase in water temperature, which presumably causes a downward turn in swimming lampreys, affected the activity in the up anddown groups differently, so that the ratio upresponses to down responses increased. We suggest that theup and down groups mediate the opposing vestibular reflexes and cause the downward and upward turns of the animal, respectively. The lamprey will stabilize the orientation in the pitch plane at which the effects of up and downgroups are equal to each other. In addition to the main test (rotation in the pitch plane), the animals were also tested by rotation in the transverse (roll) plane. It was found that 22% of RS neurons responding to pitch tilts also responded to roll tilts. The overlap between the pitch and roll populations suggests that the RS pathways are partly shared by the pitch and roll control systems.


1997 ◽  
Vol 78 (2) ◽  
pp. 960-976 ◽  
Author(s):  
Fredrik Ullén ◽  
Tatiana G. Deliagina ◽  
Grigori N. Orlovsky ◽  
Sten Grillner

Ullén, Fredrik, Tatiana G. Deliagina, Grigori N. Orlovsky, and Sten Grillner. Visual pathways for postural control and negative phototaxis in lamprey. J. Neurophysiol. 78: 960–976, 1997. The functional roles of the major visuo-motor pathways were studied in lamprey. Responses to eye illumination were video-recorded in intact and chronically lesioned animals. Postural deficits during spontaneous swimming were analyzed to elucidate the roles of the lesioned structures for steering and postural control. Eye illumination in intact lampreys evoked the dorsal light response, that is, a roll tilt toward the light, and negative phototaxis, that is a lateral turn away from light, and locomotion. Complete tectum-ablation enhanced both responses. During swimming, a tendency for roll tilts and episodes of vertical upward swimming were seen. The neuronal circuitries for dorsal light response and negative phototaxis are thus essentially extratectal. Responses to eye illumination were abolished by contralateral pretectum-ablation but normal after the corresponding lesion on the ipsilateral side. Contralateral pretectum thus plays an important role for dorsal light response and negative phototaxis. To determine the roles of pretectal efferent pathways for the responses, animals with a midmesencephalichemisection were tested. Noncrossed pretecto-reticular fibers from the ipsilateral pretectum and crossed fibers from the contralateral side were transected. Eye illumination on the lesioned side evoked negative phototaxis but no dorsal light response. Eye illumination on the intact side evoked an enhanced dorsal light response, whereas negative phototaxis was replaced with straight locomotion or positive phototaxis. The crossed pretecto-reticular projection is thus most important for the dorsal light response, whereas the noncrossed projection presumably plays the major role for negative phototaxis. Transection of the ventral rhombencephalic commissure enhanced dorsal light response; negative phototaxis was retained with smaller turning angles than normal. Spontaneous locomotion showed episodes of backward swimming and deficient roll control (tilting tendency). Transections of different spinal pathways were performed immediately caudal to the brain stem. All spinal lesions left dorsal light response in attached state unaffected; this response presumably is mediated by the brain stem. Spinal hemisection impaired all ipsiversive yaw turns; the animals spontaneously rolled to the intact side. Bilateral transection of the lateral columns impaired all yaw turns, whereas roll control and dorsal light response were normal. After transection of the medial spinal cord, yaw turns still could be performed whereas dorsal light response was suppressed or abolished, and a roll tilting tendency during spontaneous locomotion was seen. We conclude that the contralateral optic nerve projection to the pretectal region is necessary and sufficient for negative phototaxis and dorsal light response. The crossed descending pretectal projection is most important for dorsal light response, whereas the noncrossed one is most important for negative phototaxis. In the most rostral spinal cord, fibers for lateral yaw turns travel mainly in the lateral columns, whereas fibers for roll turns travel mainly in the medial spinal cord.


2002 ◽  
Vol 87 (1) ◽  
pp. 1-14 ◽  
Author(s):  
T. G. Deliagina ◽  
E. L. Pavlova

A postural control system in the lamprey is driven by vestibular input and maintains the dorsal-side-up orientation of the animal during swimming. After a unilateral labyrinthectomy (UL), the lamprey continuously rolls toward the damaged side. Normally, a recovery of postural equilibrium (“vestibular compensation”) takes about 1 mo. However, illumination of the eye contralateral to UL results in an immediate and reversible restoration of equilibrium. Here we used eye illumination as a tool to examine a functional recovery of the postural network. Important elements of this network are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections to the spinal cord. In this study, we characterized modifications of the vestibular responses in individual RS neurons caused by UL and the effect exerted on these responses by eye illumination. The activity of RS neurons was recorded from their axons in the spinal cord by chronically implanted electrodes, and spikes in individual axons were extracted from the population activity signals. The same neurons were recorded both before and after UL. Vestibular stimulation (rotation in the roll plane through 360°) and eye illumination were performed in quiescent animals. It was found that the vestibular responses on the UL-side changed only slightly, whereas the responses on the opposite side disappeared almost completely. This asymmetry in the bilateral activity of RS neurons is the most likely cause for the loss of equilibrium in UL animals. Illumination of the eye contralateral to UL resulted, first, in a restoration of vestibular responses in the neurons inactivated by UL and in an appearance of vestibular responses in some other neurons that did not respond to vestibular input before UL. These responses had directional sensitivity and zones of spatial sensitivity similar to those observed before UL. However, their magnitude was smaller than before UL. Second, the eye illumination caused a reduction of the magnitude of vestibular responses on the UL side. These two factors tend to restore symmetry in bilateral activity of RS neurons, which is the most likely cause for the recovery of equilibrium in the swimming UL lamprey. Results of this study are discussed in relation to the model of the roll control system proposed in our previous studies as well as in relation to the vestibular compensation.


1978 ◽  
Vol 41 (3) ◽  
pp. 821-834 ◽  
Author(s):  
P. W. Wyzinski ◽  
R. W. McCarley ◽  
J. A. Hobson

1. Reticulospinal neurons were identified by antidromic invasion from spinal cord electrodes chronically implanted at C4 in cats. 2. Most of the neuronal population studied lay within the medial portion of the giant cell field from the anterior pontine and to the anterior medullary reticular formation (FTG). A few cells were found in the tegmental reticular nucleus (TRC) which has not previously been known to project to the spinal cord. 3. Extracellular action potentials from the neuronal somata of the identified neurons were recorded continuously throughout naturally occurring sleep-waking cycles. 4. The identified reticulospinal neurons shared three properties, suggesting a generator function in desynchronized sleep (D) (with previously recorded but unidentified FTG neurons): selectivity (or concentration of discharge in D); tonic latency (or firing rate increases beginning several minutes prior to D); and phasic latency (or firing rate increases occurring prior to eye movements within D). 5. The location, discharge properties, and spinal projections of FTG neurons are, thus, all consistent with the hypothesis that they may directly mediate some of the descending excitatory and inhibitory influences on spinal reflex pathways in desynchronized sleep.


2011 ◽  
Vol 111 (5) ◽  
pp. 1484-1490 ◽  
Author(s):  
Jean-Sébastien Blouin ◽  
Christopher J. Dakin ◽  
Kees van den Doel ◽  
Romeo Chua ◽  
Bradford J. McFadyen ◽  
...  

Daily activities, such as walking, may require dynamic modulation of vestibular input onto motoneurons. This dynamic modulation is difficult to identify in humans due to limitations in the delivery and analysis of current vestibular probes, such as galvanic vestibular stimulation. Stochastic vestibular stimulation, however, provides an alternative method to extract human vestibular reflexes. Here, we used time-dependent coherence and time-dependent cross-correlation, coupled with stochastic vestibular stimulation, to investigate the phase dependency of human vestibular reflexes during locomotion. We found that phase-dependent activity from the medial gastrocnemius muscles is correlated with the vestibular signals over the 2- to 20-Hz bandwidth during the stance phase of locomotion. Vestibular-gastrocnemius coherence and time-dependent cross-correlations reached maximums at 21 ± 4 and 23 ± 8% of the step cycle following heel contact and before the period of maximal electromyographic activity (38 ± 5%). These results demonstrate 1) the effectiveness of these techniques in extracting the phase-dependent modulation of vestibulomuscular coupling during a cyclic task; 2) that vestibulomuscular coupling is phasically modulated during locomotion; and 3) that the period of strongest vestibulomuscular coupling does not correspond to the period of maximal electromyographic activity in the gastrocnemius. Therefore, we have shown that stochastic vestibular stimulation, coupled with time-frequency decomposition, provides an effective tool to assess the contribution of vestibular ex-afference to the muscular control during locomotion.


1986 ◽  
Vol 55 (2) ◽  
pp. 375-401 ◽  
Author(s):  
T. Drew ◽  
R. Dubuc ◽  
S. Rossignol

Recordings were made from single units in the medullary reticular formation (MRF) between AP-4.2 and AP-12.9 and from the midline to 3.7 mm lateral in chronically prepared, unrestrained cats walking on a treadmill. Recordings were made with rigid microelectrodes held in a microdrive, and reticulospinal neurons were identified by antidromic stimulation of their axons through microwires chronically implanted into the spinal cord at the L2 level. Electromyograms (EMGs) were recorded from flexor and extensor muscles of the fore- and hindlimbs as well as from back and neck muscles. In total, 295 cells were recorded from 40 penetrations in 4 cats; 252 of these cells were recorded from the more medial regions of the reticular formation encompassing the gigantocellular, magnocellular, and lateral tegmental fields; 38.5% of these (97/252) were antidromically identified from the spinal cord. The remaining 43 neurons (43/295) were recorded from a more lateral and ventral position. These medial and ventrolateral groups of neurons differed not only in position but also in aspects of their discharge during locomotion. Rank-ordered raster displays, triggered from the onset of each recorded muscle, were used to correlate neuronal and muscular activity. The discharge rate of 31% of the reticulospinal neurons (30/97) was modulated once or twice in each step cycle and was strictly related to one or more of the recorded EMGs (EMG-related neurons) on the basis of the pattern of discharge. The discharge of 33/97 (34%) of the neurons was modulated at the periodicity of the locomotor rhythm but could not be correlated with any of the recorded EMGs (locomotor-related cells), whereas the remaining 34/97 neurons (35%) were either silent, fired tonically, or were not related to the locomotor pattern (unrelated cells). Of the EMG-related neurons 27% were related to flexor muscles and the remaining 63% to extensor muscle activity. The discharge pattern of all except two of the flexor-related neurons was correlated with hindlimb muscle activity, whereas that of the extensor-related neurons was correlated almost equally with fore- and hindlimb muscles. Correlations were found with muscles lying both ipsilaterally and contralaterally to the site of the recordings. Although the locomotor-related neurons showed no preferential relation with any of the recorded EMGs, a comparison of the depth of modulation of their discharge measured from postevent histograms suggested that more of these cells were related to the forelimb than to the hindlimb.(ABSTRACT TRUNCATED AT 400 WORDS)


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