| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Biological Sciences, Marquette University, Milwaukee, Wisconsin 53233
Submitted 1 July 2003; accepted in final form 19 April 2004
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
) and is conveyed by ascending spinal pathways. Specifically, the spinocerebellar pathway sends centrally generated information from the spinal cord to the brain stem via the cerebellum (Arshavsky et al. 1978a,b; Orlovsky 1970b). Work on spinal/brain stem interactions during locomotion has been hindered, however, due to the complexity of the mammalian system. Here, the synaptic interactions between the ascending spinobulbar pathway and reticulospinal neurons of the lamprey brain stem were investigated.
In lamprey, a lower vertebrate, the locomotor pattern consists of rhythmic contractions of body muscles that alternate from side to side and propagate down the length of the body. In the in vitro lamprey spinal cord preparation, where the muscles have been removed, this same pattern can be observed in ventral root discharges and is called fictive swimming (Cohen and Wallén 1980). Bath perfusion of an excitatory amino acid can be used to generate fictive swimming in the isolated lamprey spinal cord. In more intact preparations, the swim patterns of the spinal cord are under the control of sensory inputs as well as inputs originating from the brain stem (Buchanan and Cohen 1982; Guertin and Dubuc 1997; McClellan and Grillner 1983).
Several nuclei of the brain stem contain reticulospinal neurons that constitute the main descending control pathway in the lamprey nervous system (Ronan 1989; Rovainen 1967a). The reticulospinal system in lamprey is involved in the control and initiation of locomotion (McClellan and Grillner 1984; Viana Di Prisco et al. 1997) and in postural and steering control (Fagerstedt et al. 2001; McClellan 1984; Wannier et al. 1998). Some reticulospinal neurons, mainly those of the posterior and middle rhombencephalic reticular nuclei (PRRN and MRRN, respectively), exhibit rhythmic membrane potential oscillations during fictive swimming (Kasicki and Grillner 1986; Kasicki et al. 1989). These oscillations have been shown to originate from the spinal cord (Dubuc and Grillner 1989) and presumably come from spinal neurons with axons projecting to the brain stem (i.e., spinobulbar neurons). Thus ascending spinal inputs could inform reticulospinal neurons of the state of locomotor spinal activity and thereby play a role in regulating the frequency of swimming and coordinating turning movements (Cohen et al. 1996; Vinay and Grillner 1993).
Anatomical studies in lamprey have revealed a population of spinobulbar neurons located primarily in the rostral spinal cord. The axons of these neurons project via the ventrolateral spinal lemniscal tracts (Ronan and Northcutt 1990; Vinay et al. 1998b), which mainly course ventrally and laterally through the basal plate of the brain stem, where they could potentially contact the distal dendrites of reticulospinal cells (Martin 1979). A few spinal lemniscal axons, however, travel medially where they could potentially contact the proximal dendrites and cell bodies of reticulospinal neurons (Ronan and Northcutt 1990). Extracellular stimulation of the lateral tracts in the rostral lamprey spinal cord, which contain spinobulbar axons, produced both excitatory and inhibitory responses in PRRN and MRRN cells (Vinay et al. 1998a). An early component of these responses persisted with twin pulses of 10–20 Hz, suggesting the existence of a fairly direct path from the lateral spinal columns to the reticulospinal neurons. However, this study could not rule out indirect inputs via local relay interneurons in the brain stem. This issue was addressed in the present study by reducing polysynaptic pathways in the brain stem with a high-divalent cation solution and observing membrane potential oscillations of PRRN and MRRN neurons during fictive locomotion in the spinal cord. We show that spinobulbar input to reticulospinal cells can be direct in lamprey, both excitatory and inhibitory, and thus provides a direct link between the brain stem and spinal cord.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
250 mg/l, Sigma) and were transected just caudal to the gills (I. unicuspis) or at the level of the anus (P. marinus). All muscles were cut away, and a longitudinal cut was made along the midline of the dorsal roof of the spinal canal to expose the spinal cord. The dorsal portion of the cranial casing was removed by two lateral cuts to expose the rostral spinal cord and brain stem. Dissection and storage of the tissue were done in cold Ringer solution (4–6°C) with the following composition (in mM): 91 NaCl, 2.1 KCl, 2.6 CaCl2, 1.8 MgCl2, 4.0 glucose, 20 NaHCO3, 8 HEPES (free acid), and 2 HEPES (sodium salt). The solution was bubbled with 98% O2-2% CO2, pH = 7.4.
Experiments were conducted the next day after the dissection to ensure a consistent recovery time. The preparation was pinned to the silicone elastomer (Sylgard)-lined (Dow Corning) bottom of a cooled recording chamber perfused with normal Ringer solution (8–10°C, 1 ml/min). The typical preparation consisted of the brain stem and 10–15 spinal segments for I. unicuspis and 50–70 spinal segments for P. marinus. Longer lengths were used for P. marinus to determine if the amount of spinal cord had any impact on the results. No apparent differences were observed, however, from the two preparations consistent with anatomical findings regarding cell numbers after retrograde labeling (Vinay et al. 1998b). A barrier of one to two segments in thickness was constructed of dental caulk (Reprosil; Dentsply Caulk) (for I. unicuspis) or Vaseline (for P. marinus). The barrier was typically centered between the second and third ventral roots to create a brain stem bath and a spinal cord bath (Fig. 1). For each experiment, the integrity of the diffusion barrier was tested by filling one bath with normal Ringer solution while the other bath was visually checked for leaks. Any leaks were repaired with Vaseline until no leakage was observed. In one test, when fast green dye (1%) was perfused in one bath, no diffusion of dye into the other bath was observed after 3 h. Once the barrier was made and tested, fictive swimming was induced in the spinal cord by perfusion of either 0.3 mM N-methyl-DL-aspartic acid (NMA) or 1 mM D-glutamate into the spinal cord bath. There was no significant difference observed in the results using D-glutamate versus NMA (P > 0.05, t-test).
|
when filled with potassium acetate (4 M). In some experiments, potassium chloride (4 M) was used. To record ventral root activity, the tip of a glass suction electrode (0.1 mm inner tip diameter) was placed on the ventral root near its exit point from the spinal cord, typically on the sixth to eighth ventral root. A second suction electrode (0.3 mm inner tip diameter) was placed on the dorsal surface of the spinal cord near the obex to identify the axonal projection of PRRN and MRRN cells (Fig. 1). This identification was accomplished by eliciting an action potential in a neuron cell body with intracellular current injection and detecting a one-for-one orthodromic spike in the ipsilateral cord. In some cells, averaging was necessary to detect the projection (Signal software, Cambridge Electronic Design or CED). All cells included in the study were confirmed as reticulospinal neurons and had intracellular action potentials of 
70 mV in base-to-peak amplitude [range = 70–120 mV; mean = 95 ± 16 (SD) mV]. The mean resting potential of all cells was –71 ± 9 mV, which was similar to resting potential in other studies done on reticulospinal neurons (Brocard and Dubuc 2003; Rouse et al. 1998; Wickelgren 1977). Intracellular signals were low-pass filtered at 3 kHz, and extracellular signals were filtered with a differential AC amplifier (A-M Systems) at 100 Hz (high-pass filter) and 1 kHz (low-pass filter). Digitizing was done with a Micro1401 ADC converter (CED) at 6 kHz for intracellular and 2 kHz for extracellular recordings. The membrane potential of reticulospinal cells was recorded in 2-min blocks with a personal computer (Spike2 software, CED) and stored on disk. Some recordings were stored on digital audiotape (Bio-Logic) and later converted to Spike2 files.
A high-divalent cation solution, composed of 20 mM Ca2+ and 5.8 mM Mg2+, was applied to the brain stem. The high-divalent cation concentration raises spike threshold (Frankenhaeuser and Hodgkin 1957) and thereby reduces conduction in polysynaptic pathways. This effect has been observed in lamprey using 20 mM Ca2+ but was accompanied by an increase in monosynaptic responses (Rovainen 1974b). Therefore 5.8 Mg2+ was used in addition to 20 mM Ca2+ because this gave a reduction of polysynaptic responses without enhancing monosynaptic responses. Reticulospinal neurons in the PRRN and MRRN were recorded intracellularly before and after addition of the high-divalent cation solution. For six cells in the PRRN in three different preparations, the impalement was maintained while the normal Ringer solution surrounding the brain stem was replaced by the high-divalent cation solution. An additional four PRRN neurons, in three preparations of similar length, were maintained during perfusion of a high-divalent, strychnine solution. Other PRRN and MRRN neurons were randomly impaled before and after solutions were replaced. For these randomly impaled neurons, averages of membrane potential during fictive swimming were obtained by triggering from the manually marked beginnings of ventral root bursts of 30 consecutive swim cycles for each neuron (Spike 2 software). The averages were then used to measure membrane potential oscillation amplitude by measuring the peak membrane potential of the crest and subtracting the potential obtained from the trough. For the PRRN cells that were continuously held before and after addition of high-Ca2+, -Mg2+ to the brain compartment, measurements of amplitude were done cycle by cycle to make a statistical comparison. The mean membrane potential value for 50 ms windows surrounding the peaks and troughs of 20 consecutive swim cycles were measured and subtracted to obtain membrane potential oscillation amplitudes for each neuron. This was done before and after high-divalent treatment.
All statistical analysis was done with SigmaStat software (SPSS). To compare two groups, such as with the pooled oscillation data, a t-test was applied. If a normality or equal variance test failed, a Mann-Whitney rank sum test was used (i.e., Fig. 4). Two groups were considered statistically different if one of the preceding tests was P 
0.05. For paired data, such as for the individually held PRRN neurons (as a group, bin 7 in Fig. 6), a paired t-test was used with the same stringency.
|
|
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
To determine whether locomotor-related spinal inputs to reticulospinal neurons are monosynaptic, a high-divalent cation solution (20 mM Ca2+, 5.8 mM Mg2+) was used to reduce conduction in polysynaptic pathways with relatively little alteration of monosynaptic potentials. In two types of experiments, the efficacy of the high-divalent solution in blocking polysynaptic activity was tested. In the first experiment, the synaptic potentials produced in a giant interneuron by a dorsal cell were tested using paired intracellular recordings. Rovainen (1967b, 1974a) demonstrated that dorsal cells, which are primary mechanosensory cells, produce both mono- and polysynaptic excitatory potentials in giant interneurons. In the example of Fig. 2A, action potentials evoked in a dorsal cell by intracellular current injection produced excitatory postsynaptic potentials (EPSPs) in a nearby (3 mm) ipsilateral giant interneuron. The composite EPSP consisted of an early response (*) and a late response (Fig. 2A1). The early response was likely monosynaptic due to the short synaptic delay (2 ms) remaining after subtraction of the dorsal cell action potential conduction time (3 ms). The late response, beginning at 20 ms, was polysynaptic due to the longer latency and the variable onset and trajectory. An additional late response sometimes occurred at 100 ms. In the high-divalent cation solution, the response beginning at 20 ms was largely abolished (Fig. 2A2), while the amplitude of the early component was reduced by only 13%. A total of six dorsal cell-giant interneuron pairs in three preparations were tested in this manner. The amplitudes of the polysynaptic components for the six pairs were significantly different after application of high-divalent cation (paired t-test, P = 0.02; mean reduction = 62 ± 17%). The monosynaptic components were also significantly different (paired t-test, P = 0.03; mean reduction = 16 ± 3%) but by a smaller percentage. When compared with each other, the percent reductions for the polysynaptic components and the monosynaptic components were statistically different (paired t-test, P = 0.002).
|
). The amplitude of this response was reduced by 80%, from 7.0 to 1.4 mV, when the high-divalent cation solution was applied to the bath surrounding the brain stem (Fig. 2B2) with no change in the ascending volley rostral to the barrier (not shown). Amplitude of oscillations in high-divalent cation solution
Neurons in the PRRN and MRRN have previously been shown to exhibit rhythmic membrane potential oscillations that are time-locked with ventral root bursting (Dubuc and Grillner 1989; Kasicki and Grillner 1986; Kasicki et al. 1989), but the directness of the spinal inputs producing these oscillations had not been tested. Because the high-divalent cation solution effectively reduced polysynaptic inputs, this solution was applied to the brain stem to test the directness of spinal inputs to reticulospinal cells during fictive locomotion. With fictive swimming activity in the spinal cord and high-divalent cation solution applied to the brain stem, PRRN (Fig. 3A) and MRRN (Fig. 3B) neurons still exhibit oscillations of membrane potential that are time-locked to the ventral root bursting.
|
Similar experiments were done on neurons in the MRRN. In a sample of nine MRRN neurons in normal Ringer solution, all nine had membrane potential oscillations during fictive swimming in the spinal cord (mean amplitude = 0.73 ± 0.61 mV, n = 9). In the high-divalent cation solution, 14 neurons were recorded, and all exhibited rhythmic membrane potential oscillations (mean amplitude = 0.56 ± 0.48 mV, n = 14). The oscillation amplitude was not significantly different in high-divalent cation solution (P = 0.59, Mann-Whitney rank-sum test; Fig. 4B). Also, the mean amplitude of membrane potential oscillations of MRRN neurons was not significantly different from that in PRRN neurons (P = 0.20, t-test).
In some experiments, PRRN neurons recorded in normal Ringer were held continuously during the change of the brain stem bath to high-divalent cation solution. Figure 5 shows the averaged membrane potentials of one such neuron before and after high-divalent cation solution. Of the six neurons recorded in this manner, four showed no significant change in membrane potential oscillation amplitude with the solution change (Fig. 6), whereas two neurons did show significant changes in amplitude. One of these showed an increase in the amplitude of membrane potential oscillations from 3.22 ± 0.85 to 4.13 ± 0.87 mV (P = 0.002, t-test; cell 2 of Fig. 5 and 6). In the second neuron, amplitude decreased from 0.73 ± 0.24 to 0.34 ± 0.13 mV (P < 0.001, t-test; cell 6 of Fig. 6). As a group, the six neurons had a mean amplitude of 1.65 ± 1.15 mV in control Ringer solution and 1.66 ± 1.47 mV in the high-divalent cation solution, and these values were not significantly different (P = 0.97, paired t-test).
|
The presence of oscillations in PRRN and MRRN cells in high-divalent cation solution supports the hypothesis that these neurons receive synaptic inputs directly from the spinal cord during fictive swimming. To determine whether or not inhibitory inputs play a role in producing these oscillations, 4 M potassium chloride electrodes were used to inject Cl– into four PRRN neurons in the high-Ca2+, -Mg2+ solution. Chloride injection has previously been shown to reverse IPSPs in lamprey spinal neurons during fictive swimming (Kahn 1982; Russell and Wallén 1983) due to a shift in the equilibrium potential for Cl–. In one PRRN neuron, a hyperpolarizing phase (Fig. 7A1) was reversed by hyperpolarizing current during chloride injection (Fig. 7A2) suggesting IPSPs. In another PRRN neuron, after Cl– injection, there was a small depolarizing peak at the end of the ipsilateral ventral root burst that was similarly enhanced when the neuron was hyperpolarized. In two other PRRN neurons, there was a reduction in oscillation amplitude after 10 min of Cl– injection (not shown) by 20% in one cell and 80% in the other, suggesting a Cl–-mediated component.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
The oscillations observed in this study were small (1 mV) when compared with rhythmic activity in PRRN and MRRN neurons during brain-stem-evoked fictive swimming. Under such conditions, i.e., when swimming was evoked by trigeminal nerve stimulation, PRRN and MRRN neurons had large membrane potential oscillations (>10 mV) and often exhibited action potentials during the depolarizing phase (Kasicki and Grillner 1986; Kasicki et al. 1989). The source of the rhythmic modulation was unclear, however, as inputs could have arisen from the brain stem and/or the spinal cord. To determine the source of rhythmic input to reticulospinal cells, Dubuc and Grillner (1989) pharmacologically activated fictive swimming in the spinal cord while keeping the brain stem quiescent as was done in the present study. Under these conditions, reticulospinal neurons showed rhythmic activity, although membrane potential oscillations were small (2 mV) and nonspiking. The source of the additional input to reticulospinal neurons during brain-stem-evoked fictive locomotion is unknown at present, but there are at least two possibilities. First, local brain stem networks could be recruited to enhance rhythmic input to neurons of the PRRN and MRRN. Second, spinal circuits could be more strongly activated resulting in a stronger activation of reticulospinal neurons. A combination of these possibilities, however, is likely.
In addition to the reticular nuclei studied here, the lamprey brain also has an anterior rhombencephalic reticular nucleus (ARRN) and a mesencephalic reticular nucleus (MRN). Whether reticulospinal neurons in these more rostral nuclei receive rhythmic inputs from the spinal cord is not known and was not tested in the present study. An anatomical study of ascending spinal pathways in lamprey showed that relatively few spinal lemniscal fibers reach the rostral region of the rhombencephalon (Ronan and Northcutt 1990), making it unlikely that there are direct spinobulbar inputs to neurons in the ARRN. Moreover, no spinal lemniscal fibers reach beyond the isthmus and into the mesencephalon (Ronan and Northcutt 1990), making it less likely for MRN neurons to receive similar input. Direct spinal inputs cannot be entirely ruled out, however, because the large Müller cells located in these nuclei (I1, M1–3) showed some indication of rhythmic activity during brain-stem-evoked fictive locomotion (Kasicki and Grillner 1986). One putative source of this input is the spinal cord. Whether or not reticulospinal neurons in these rostral nuclei receive rhythmic signals from the spinal cord during fictive locomotion needs to be established before the directness of such input is proposed. Also, smaller reticulospinal neurons in the ARRN and MRN have not been tested.
Descending control pathways including the reticulospinal pathway were first well characterized in the cat. Unit recordings from reticulospinal (Drew et al. 1986; Orlovsky 1970a), vestibulospinal (Orlovsky 1972a), and rubrospinal (Orlovsky 1972b) neurons showed rhythmic activity during locomotion that was coordinated with one or more limbs. Furthermore, the rhythmic activity was not changed by the absence of peripheral sensory information (Arshavsky et al. 1978a,b), indicating that central nervous mechanisms were the source of the input. Lundberg (1971) advanced the idea that the ventral spinocerebellar tract could convey such centrally generated activity to centers of the brain stem and enable them to monitor the activity of spinal interneurons during locomotion. It was also found that the rhythmic activity of descending neurons during locomotion was completely dependent on the presence of the cerebellum (Orlovsky 1970b). This suggests that rather than a direct path to descending systems, the ascending signals in cat are transmitted via the cerebellum, where they are integrated with other signals. In addition, Arshavsky et al. (1986) suggested that ascending information was greatly reduced by the cerebellum, thus informing descending control centers of only the critical components of the locomotor pattern. Supraspinal structures may then be continually informed of activity in the spinal cord yet utilize this information only when necessary. For example, if an obstacle is encountered, or a perturbation of locomotion occurs (e.g., changing surface), the brain stem would know the current activity of the spinal cord to appropriately adjust the motor pattern under the new circumstances.
In lamprey, ascending signals also relay information about the activity of the spinal locomotor network to the brain stem during fictive locomotion. Unlike in cat, however, this input can be direct to reticulospinal neurons. The directness of ascending inputs in lamprey is consistent with the lack of a clearly defined cerebellum and with the lack of affect on rhythmic activity in reticulospinal neurons on removal of the isthmic region of the cerebellum (Kasicki et al. 1989). As in cat, the presumed function of this ascending input in lamprey is to inform the descending systems about the current state of the locomotor network. Such information would be important in regulating speed and turning and in responding to unexpected perturbations during swimming. One approach to understanding the function of ascending spinal feedback is a detailed mapping of the connectivity and activity patterns between the spinal cord and brain stem that could provide a framework for studying the functional organization of ascending/descending systems. To this end, the relative directness of ascending inputs to the descending neurons in lamprey may offer an advantageous preparation for such studies.
The partial reduction of oscillation amplitude by strychnine in high-divalent cation solution supports the hypothesis that both direct excitatory and inhibitory spinal inputs create the membrane potential oscillations in lamprey PRRN neurons. Strychnine blocks Cl–-mediated IPSPs that are glycinergic in reticulospinal neurons (Dubuc et al. 1993; Matthews and Wickelgren 1979; Vinay et al. 1998a). Thus a partial reduction indicates that strychnine-sensitive IPSPs are involved but that a rhythmic excitatory component may also be present. Alternatively, GABA-mediated IPSPs could be involved. Although GABA has been shown to hyperpolarize reticulospinal cells and to presynaptically modulate synaptic inputs (Dubuc et al. 1993; Vinay et al. 1998a; Wickelgren 1977), Matthews and Wickelgren (1979) showed that inhibitory inputs to reticulospinal neurons were more sensitive to strychnine than to picrotoxin or bicuculline, suggesting that glycine is the main transmitter mediating inhibitory responses in reticulospinal neurons. This suggests that residual oscillations after strychnine application are caused by excitatory inputs and not by failure to block GABA-mediated IPSPs. Alternating excitatory and inhibitory inputs have been shown to underlie membrane potential oscillations in lamprey spinal neurons during fictive swimming (Kahn 1982). This input is conveyed directly to spinal neurons via identified premotor interneurons such as the contralateral, caudal inhibitory interneurons (CCIN) and the excitatory interneurons (EIN) (Buchanan 1982; Buchanan et al. 1989). The present study implicates a population of spinal neurons in providing inputs directly to reticulospinal neurons. These spinobulbar neurons may be similar to CCINs and EINs in that there are both inhibitory and excitatory neurons that are rhythmically active during fictive locomotion.
To summarize, the results of the present study support the conclusion that, in lamprey, nerve cells of the spinal cord connect directly with reticulospinal neurons in the PRRN and MRRN and thereby form a direct spino-reticulo-spinal loop. Reticulospinal neurons constitute the main descending control pathway in lamprey and can affect the frequency of fictive locomotion and the intensity of ventral root bursting and are presumably involved in steering and postural control (Buchanan and Cohen 1982; McClellan and Grillner 1984; Wannier et al. 1998). The membrane potential oscillations of PRRN and MRRN cells that are created by spinal inputs provide information regarding the state of the spinal locomotor networks, thus putatively influencing reticulospinal neurons and their control of locomotion.
|
GRANTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
ACKNOWLEDGMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: J. T. Buchanan, Dept. of Biological Sciences, Marquette University, P.O. Box 1881, Milwaukee, WI 53201 (E-mail: james.buchanan{at}marquette.edu).
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
Arshavsky YI, Gelfand IM, Orlovsky GN, and Pavlova GA. Messages conveyed by descending tracts during scratching in the cat. I. Activity of vestibulospinal neurons. Brain Res 159: 99–110, 1978a.[CrossRef][ISI][Medline]
Arshavsky YI, Gelfand IM, Orlovsky GN, and Pavlova GA. Messages conveyed by descending tracts during scratching in the cat. II. Activity of rubrospinal neurons. Brain Res 159: 111–123, 1978b.[CrossRef][ISI][Medline]
Brocard F and Dubuc R. Differential contribution of reticulospinal cells to the control of locomotion induced by the mesencephalic locomotor region. J Neurophysiol 90: 1714–1727, 2003.
Buchanan JT. Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophysiol 47: 961–975, 1982.
Buchanan JT and Cohen AH. Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation. J Neurophysiol 47: 948–960, 1982.
Buchanan JT, Grillner S, Cullheim S, and Risling M. Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. J Neurophysiol 62: 59–69, 1989.
Cohen AH, Guan L, Harris J, Jung R, and Kiemel T. Interaction between the caudal brainstem and the lamprey central pattern generator for locomotion. Neuroscience 74: 1161–1173, 1996.[ISI][Medline]
Cohen AH and Wallén P. The neuronal correlate of locomotion in fish: "fictive swimming" induced in an in vitro preparation of the lamprey spinal cord. Exp Brain Res 41: 11–18, 1980.[ISI][Medline]
Drew T, Dubuc R, and Rossignol S. Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. J Neurophysiol 55: 375–401, 1986.
Dubuc R, Bongianni F, Ohta Y, and Grillner S. 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, 1993.[CrossRef][ISI][Medline]
Dubuc R and Grillner S. The role of spinal cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey. Brain Res 483: 196–200, 1989.[CrossRef][ISI][Medline]
Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, and Ullén F. Lateral turns in the lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns. J Neurophysiol 86: 2257–2265, 2001.
Frankenhaeuser B and Hodgkin AL. The action of calcium on the electrical properties of squid axons. J Physiol 137: 218–244, 1957.
Guertin P and Dubuc R. Effects of stimulating the reticular formation during fictive locomotion in lampreys. Brain Res 753: 328–334, 1997.[CrossRef][ISI][Medline]
Kahn J. Patterns of synaptic inhibition in motoneurons and interneurons during fictive swimming in the lamprey, as revealed by Cl– injections. J Comp Physiol 147: 189–194, 1982.[CrossRef]
Kasicki S and Grillner S. Müller cells and other reticulospinal neurones are phasically active during fictive locomotion in the isolated nervous system of the lamprey. Neurosci Lett 69: 239–243, 1986.[CrossRef][ISI][Medline]
Kasicki S, Grillner S, Ohta Y, Dubuc R, and Brodin L. Phasic modulation of reticulospinal neurons during fictive locomotion and other types of spinal motor activity in lamprey. Brain Res 484: 203–216, 1989.[CrossRef][ISI][Medline]
Lundberg A. Function of the ventral spinocerebellar tract. A new hypothesis. Exp Brain Res 12: 317–330, 1971.[ISI][Medline]
Martin RJ. A study of the morphology of the large reticulospinal neurons of the lamprey ammocoete by intracellular injection of procion yellow. Brain Behavior Evol 16: 1–18, 1979.[ISI][Medline]
Matthews G and Wickelgren WO. Glycine, GABA and synaptic inhibition of reticulospinal neurons of lamprey. J Physiol 293: 393–415, 1979.
McClellan AD. Descending control and sensory gating of ‘fictive’ swimming and turning responses elicited in an in vitro preparation of the lamprey brain stem/spinal cord. Brain Res 302: 151–162, 1984.[CrossRef][ISI][Medline]
McClellan AD and Grillner S. Initiation and sensory gating of "fictive" swimming and withdrawal responses in an in vitro preparation of the lamprey spinal cord. Brain Res 269: 237–250, 1983.[CrossRef][ISI][Medline]
McClellan AD and Grillner S. Activation of "fictive swimming" by electrical microstimulation of brain stem locomotor regions in an in vitro preparation of the lamprey central nervous system. Brain Res 300: 357–361, 1984.[CrossRef][ISI][Medline]
Orlovsky GN. Work of the reticulo-spinal neurons during locomotion. Biophysics 15: 761–771, 1970a.
Orlovsky GN. Influence of the cerebellum on the reticulo-spinal neurons during locomotion. Biophysics 15: 928–936, 1970b.
Orlovsky GN. Activity of vestibulospinal neurons during locomotion. Brain Res 46: 85–98, 1972a.[CrossRef][ISI][Medline]
Orlovsky GN. Activity of rubrospinal neurons during locomotion. Brain Res 46: 99–112, 1972b.[CrossRef][ISI][Medline]
Ronan M. Origins of the descending spinal projections in petromyzontid and myxinoid agnathans. J Comp Neurol 281: 54–68, 1989.[CrossRef][ISI][Medline]
Ronan M and Northcutt RG. Projections ascending from the spinal cord to the brain in petromyzontid and myxinoid agnathans. J Comp Neurol 291: 491–508, 1990.[CrossRef][ISI][Medline]
Rouse DT, Quan X, and McClellan AD. Biophysical properties of descending brain neurons in larval lamprey. Brain Res 779: 301–308, 1998.[CrossRef][ISI][Medline]
Rovainen CM. Physiological and anatomical studies on large neurons of the central nervous system of the sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. J Neurophysiol 30: 1000–1023, 1967a.
Rovainen CM. Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). II. Dorsal cells and giant interneurons. J Neurophysiol 30: 1024–1042, 1967b.
Rovainen CM. Synaptic interactions of identified nerve cells in the spinal cord of the sea lamprey. J Comp Neurol 154: 189–206, 1974a.[CrossRef][ISI][Medline]
Rovainen CM. Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey. J Comp Neurol 154: 207–224, 1974b.[CrossRef][ISI][Medline]
Russell DF and Wallén P. On the control of myotomal motoneurons during "fictive swimming" in the lamprey spinal cord in vitro. Acta Physiol Scand 117: 161–170, 1983.[ISI][Medline]
Viana Di Prisco G, Pearlstein E, Robitaille R, and Dubuc R. Role of sensory-evoked NMDA plateau potentials in the initiation of locomotion. Science 278: 1122–1125, 1997.
Vinay L, Bongianni F, Ohta Y, Grillner S, and Dubuc R. Spinal inputs from lateral columns to reticulospinal neurons in lampreys. Brain Res 808: 279–293, 1998a.[CrossRef][ISI][Medline]
Vinay L, Bussières N, Shupliakov O, Dubuc R, and Grillner S. Anatomical study of spinobulbar neurons in lampreys. J Comp Neurol 397: 475–492, 1998b.[CrossRef][ISI][Medline]
Vinay L and Grillner S. The spino-reticulo-spinal loop can slow down the NMDA-activated spinal locomotor network in lamprey. Neuroreport 4: 609–612, 1993.[ISI][Medline]
Wannier T, Deliagina TG, Orlovsky GN, and Grillner S. Differential effects of the reticulospinal system on locomotion in lamprey. J Neurophysiol 80: 103–112, 1998.
Wickelgren WO. Physiological and anatomical characteristics of reticulospinal neurones in lamprey. J Physiol 270: 89–114, 1977.
This article has been cited by other articles:
|
|
 |
|
  R. W. Smetana, S. Alford, and R. Dubuc Muscarinic Receptor Activation Elicits Sustained, Recurring Depolarizations in Reticulospinal Neurons J Neurophysiol, May 1, 2007; 97(5): 3181 - 3192. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Einum and J. T. Buchanan Spinobulbar Neurons in Lamprey: Cellular Properties and Synaptic Interactions J Neurophysiol, October 1, 2006; 96(4): 2042 - 2055. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Einum and J. T. Buchanan Membrane Potential Oscillations in Reticulospinal and Spinobulbar Neurons During Locomotor Activity J Neurophysiol, July 1, 2005; 94(1): 273 - 281. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
