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Previous Article | Next Article
The Journal of Neuroscience, May 15, 2002, 22(10):4229-4240
Sensory Activation and Role of Inhibitory Reticulospinal Neurons that Stop Swimming in Hatchling Frog Tadpoles
Ray Perrins, Alison Walford, and Alan Roberts School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Activity in neuronal networks underlying locomotion and other rhythmic actions can start and stop in response to specific sensory stimuli. In vertebrate locomotion, some reticulospinal neurons such as Mauthner neurons can initiate activity, but the neurons controlling stopping are not defined. We have studied swimming in tadpoles of the frog, Xenopus, which is started by touching the skin and stops when the head contacts a solid surface. Using an immobilized tadpole preparation, the same stimuli control fictive swimming. When head contact is imitated by pressure to the head skin sensory neurons in the trigeminal ganglion are active, spinal neurons receive GABAergic inhibition, and swimming stops. Here we record intracellularly from neurons in the hindbrain that are excited by pressure or electrical stimulation to the head skin. By intracellular filling with neurobiotin, we identify these anatomically as mid-hindbrain reticulospinal neurons (MHRs). These have contralateral descending projections to the spinal cord and GABA-like immunoreactivity. They are rhythmically inhibited during fictive swimming. Individual MHRs reliably stopped ongoing swimming when brief firing was induced by intracellular current injection. The ability of individual MHRs to stop swimming was blocked by the GABAA antagonist bicuculline. Our evidence indicates that MHRs receive direct excitation from trigeminal sensory neurons and in turn release GABA to directly inhibit spinal neurons and turn off the swimming central pattern generator.
Key words: locomotion; central pattern generator; trigeminal; GABA; Xenopus; brainstem
INTRODUCTION
Locomotion needs to be started and stopped in response to specific behavioral cues. It is known that specific stimuli can stop locomotion in a range of animals (dogfish: Gray and Sand, 1936
; insects: Fraenkel, 1932
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Figure 1. The preparation used for studying hindbrain neurons and their spinal targets. A, The immobilized tadpole is pinned on its right side. Swimming is started using a stimulating electrode on the tail skin and motor output monitored using a suction ventral root (VR) electrode. Intracellular recordings can be made from the hindbrain (as illustrated) or the spinal cord. Drugs are applied to neurons via a microperfusion system. Pressure is applied to the head using a glass probe. B, The glass probe is attached to a loudspeaker via a lever pivoting about the point indicated. The half-sinusoid shape of the input to the loudspeaker is shown.
In Xenopus tadpoles swimming normally stops when the tadpole contacts an object or the water surface with its head (Roberts and Blight, 1975
The purpose of this study was to characterize the anatomy and physiology of reticulospinal neurons excited by pressing the head skin and to obtain evidence for their role in stopping swimming. For the first time in any system, we have defined the role of a class of inhibitory reticulospinal neuron.
MATERIALS AND METHODS
Recordings were made from 78 hatchling tadpoles of Xenopus laevis (developmental stage 37-38; Nieuwkoop and Faber, 1956
-bungarotoxin (10 µM). The tadpoles were left in
Microelectrodes with DC resistances of 150-250 M
were pulled on a Sutter P-97 microelectrode puller and filled with 3 M potassium acetate or 2 M potassium acetate with 1% Neurobiotin (Molecular Probes, Eugene, OR). Neurons were impaled using a Burleigh PZ-100 piezoelectric step driver and using capacitance overcompensation. Neurons were used if they had a stable resting potential more negative than
50 mV and showed clear rhythmic synaptic input during fictive swimming (Boothby and Roberts, 1992b
After testing their physiological responses, neurobiotin (Vector Laboratories, Burlingame, CA) was injected into the neurons using positive 0.5 sec duration current pulses of 0.1-0.3nA applied once per second for 5-10 min. The electrode was then withdrawn, and the animals were left for 30-60 min for the dye to spread throughout the neuron, before being fixed in 2% gluteraldehyde in phosphate buffer (PB; 0.08 M Na2HPO4 and 0.02 M NaH2PO4, pH 7.4) for 2 hr at room temperature. After fixation the dorsal parts of the axial muscles were removed from the right side of the animal to facilitate later processing. The preparation was washed in PBS (120 mM NaCl in phosphate buffer, pH 7.4) for 1 hr with two changes of solution. The preparation was then washed in PBS containing 1% Triton X-100 for 1 hr with two changes of solution and then incubated for 3 hr in a solution of PBS containing 0.5% Triton and a 1:200 dilution of ExtrAvidin (Sigma). After washing with three changes of PBS for 1 hr, the preparation was placed in 0.05% diaminobenzidine (DAB) in PBS for 5 min, and then into a solution of 0.05 DAB 0.03% hydrogen peroxide for 2-5 min. When the neurons became visible, the reaction was stopped by transferring to PBS. The CNS, with notochord and ventral axial muscles attached, was then dissected out of the preparation and dehydrated, cleared in methyl benzoate and xylene, and mounted on its side in DePeX between coverslips so that it could be examined from both sides. Neurons were drawn using a camera lucida and photographed using a Nikon Coolpix 990 digital camera. Because the mid-hindbrain reticulospinal neurons (MHRs) filled had a contralateral axon, photos were taken at several different focal planes, and then the images were processed and stacked using Adobe Photoshop software. Because specimens shrink by ~22% during dehydration (Li et al., 2001
In immobilized animals, the stopping pathway was stimulated by pressing the head skin at the region of the cement gland using a 0.5 mm diameter rounded glass probe (Fig. 1). The probe was attached, via a lever, to a loudspeaker (Roberts and Blight, 1975
Data were stored using Signal software in conjunction with a Cambridge Electronic Design 1401 computer interface. Current was injected into neurons via the recording electrode. All measures are mean ± SD.
Drugs used:
RESULTS
Characterization of hindbrain neurons responding to pressing the cement gland
Morphology
Ten neurons that responded to pressing the cement gland (see below) were filled successfully with neurobiotin. Figure 2 shows a composite photograph of a typical filled neuron. Figure 3 shows drawings of three examples at both low and high power, whereas Figure 4 shows all 10 neurons schematically. In a further two cases partial fills were achieved (with only cell body and part of the initial axon segment visible). The cell bodies of the neurons were situated near the dorsoventral midline, in the caudal hindbrain, in the region adjacent to the first and second post-otic myotomes (400-550 µm from the midbrain, approximately equivalent to the sixth to eighth rhombomeres) (Fig. 3). The somata were dorsoventrally elongated (mean height, 28 ± 3 µm; mean width, 17 ± 4 µm; n = 9). All neurons were multipolar, usually with a few, short dorsally projecting dendrites and several elongated, ventral dendrites. All neurons had a contralateral, descending axon between 800- and 1700-µm-long (mean, 1180 ± 350 µm; n = 8) (Fig. 4). In addition to this, two examples had ipsilateral descending axons (1140 and 1240 µm long) and two had shorter contralateral ascending axons (20 and 280 µm in length). Some lengths may be underestimates where axons did not show a distinct end-bulb and may therefore be incompletely filled.
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Figure 2. Photomontage of an MHR neuron filled with neurobiotin and also shown in Figure 3, A and D. Part of the hindbrain near its border with the spinal cord (*) is shown viewed from the left side in a whole mount of the CNS. Rostral is to the left. The pear-shaped MHR soma has a ventral principal process with dendrites (e.g., relatively long ventral dendrite at arrowhead) and an axon that crosses ventrally and then descends on the opposite side (arrow). Short, thick arrows indicate the dorsal and ventral edges of the hindbrain.
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Figure 3. Anatomy of MHR neurons. A-C, Scale drawings of a lateral view of the CNS showing the overall anatomy of three neurobiotin filled MHRs. P, Pineal gland; Trig, trigeminal nerve; f, forebrain; m, midbrain; h, hindbrain. Asterisk indicates border of hindbrain and spinal cord. Post-otic myotomes are numbered. D-F, The region of the soma in lateral view of the same three neurons. Rostral is to the left. Note the relatively long ventral dendrites (arrowheads) and crossed, descending axon. Arrows indicate the point where the axon crosses the ventral midline of the CNS. c, Contralateral axon; i, ipsilateral axon.
The neurons share the following features with GABA-immunopositive MHRs, as described in Roberts et al. (1987)
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Figure 4. Schematic representation of the 10 MHR neurons filled by intracellular injection of neurobiotin. The top neuron is superimposed on a diagram of the CNS (viewed dorsally) showing hindbrain, spinal cord, trigeminal nerve (Trig.), otic capsule and numbered myotomes. The remaining neurons are shown to the same scale, and the distance in millimeters from the mid-hindbrain boundary is shown at the bottom. A dashed line shows the nominal boundary between the hindbrain and spinal cord. Most axons faded at their distal end, but four ended in growth cones, shown by small, black rectangles. Note the limited rostrocaudal distribution of somata.
Neuronal properties
The mean resting potential for MHRs was
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Figure 5. Firing properties of MHRs. A, B, Firing responses of two neurons to current pulses from 0.1 to 0.35 nA in 0.05 nA steps. C, Graph showing firing frequency against injected current for eight MHRs. Closed circles are instantaneous firing frequency for the first two spikes. Open circles are frequency measured over the whole 100 msec current pulse. Both are fitted with exponential curves.
Responses of MHRs to activation of pathways that start fictive swimming
We investigated the responses of MHRs to two different types of input that can start swimming in Xenopus tadpoles. The first of these involves the pineal eye, which is excited by light dimming and can initiate swimming (Foster and Roberts, 1982
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Figure 6. Response of MHR to light dimming over pineal eye. When the light level drops, swimming is initiated and recorded as rhythmic ventral root (VR) bursts. In intracellular record from MHR (MHR) no excitation is seen, but midcycle IPSPs are present on every cycle during swimming.
The second type of input investigated was electrical stimulation of the trunk skin, which stimulates the touch pathway to initiate swimming. The stimulating electrode was placed on the skin at the level of the anus, and after a 0.5 msec stimulus above the threshold for swimming, several distinct types of input to MHRs were observed (Fig. 7A,C): (1) An EPSP with a short, fixed latency. This was revealed more clearly when glycinergic inhibition was blocked by strychnine (Fig. 7C). The overall latency of this EPSP was 10.8 ± 1.6 msec (n = 81 EPSPs from five preparations). However, the variance of the delay in each preparation was very small (~0.1 msec) (Table 1) and was consistent with a monosynaptic connection (see Discussion). In 2 of 12 cases there were also indications of a short-latency IPSP remaining in strychnine, indicated by a sharp cutoff to the EPSP and the membrane potential going below the resting potential (seen in Fig. 7A but not in 7C). Because this strychnine-resistant IPSP was not a reliable input, it was not investigated further. (2) EPSPs with long, variable latencies. These were observed in seven of eight neurons tested. The EPSPs occurred during swimming between 100 msec and 1 sec after the stimulus. They occurred at all phases of swimming, apparently at random (compared with ipsilateral ventral root discharge) (Fig. 7B). The total number of these EPSPs did seem to increase with increasing stimulus intensity, but we have not investigated these EPSPs further in this study. (3) Reliable, midcycle IPSPs. These were seen throughout swimming episodes (Figs. 6, 7A). The IPSPs were only seen at midcycle, compared with ipsilateral ventral root discharge, and were reversibly blocked by the glycine antagonist strychnine (1 µM; n = 6) (Fig. 7A). The midcycle IPSPs were very reliable, occurring on 100% of cycles (measured on 100 cycles each from six MHRs). This is in contrast to IPSPs in spinal sensory dorsolateral commissural interneurons that tend to fail on some cycles as swimming progresses (Sillar and Roberts, 1992
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Figure 7. MHR neurons receive excitation after trunk skin stimulation. A, In control, two types of excitation can be seen when the stimulus (at artifact, asterisk) initiates fictive swimming (seen in ventral root record, VR), a short-latency EPSP (arrows) and longer, variable, latency EPSPs (arrowheads). The inhibition consists of reliable, midcycle IPSPs (dashed lines). Strychnine reversibly blocks the midcycle IPSPs and reveals the excitation more clearly. Note that in strychnine the short-latency EPSP is cut off, and there is a subsequent undershoot below the resting potential, indicating a short-latency IPSP (open arrow). This was only seen in 2 of 12 preparations (compare with C, from another preparation). Bi, The number of long-latency EPSPs occurring at different phases of the swimming cycle. No phasic relationship can be seen. Bii, In contrast, the IPSPs during swimming are centered around 0.5 phase (midcycle). C, Five traces in control and five in strychnine reveal the short-latency EPSP in response to tail skin stimulation. Note the low variability of the delay to the onset of the EPSP.
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Table 1. Delays and variances (both in msec) to events after brief (1 msec) electrical skin stimulation Responses of MHRs on activation of the stopping pathway
When the head skin was pressed to stop fictive swimming, MHRs received excitation and usually fired one or more action potentials (Fig. 8). MHRs also received excitation (a barrage of EPSPs) when the cement gland was pressed in the absence of swimming (Fig. 9A). The excitation was graded with stimulus intensity (n = 6) (Fig. 9A), and if the stimulation was strong enough, resulted in firing. Instantaneous firing frequencies in response to pressing the cement gland could reach >100 Hz, approximately equivalent to 0.35 nA injected current (twice the threshold current) (Fig. 5). The excitation was reversibly blocked by the broad spectrum excitatory amino acid (EAA) antagonist kynurenate (1 mM; n = 6) (Fig. 9A). Repeated pressing of the cement gland resulted in responses that steadily reduced in both duration and amplitude (n = 4) (Fig. 9B).
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Figure 8. MHR activity during swimming and head press. A, Examples from two preparations. In each case swimming is started by a 1 msec duration electrical stimulus to the trunk skin (at asterisk) and is monitored from the ventral roots (VR). During swimming MHRs receive rhythmic, reliable IPSPs. Swimming is stopped by pressing the head skin (cement gland), when the MHRs receive excitation and fire action potentials. The anatomy of the first neuron is shown in Figure 2, A and D, the second in Figure 2, B and E. B, The input to the lower MHR shown at an expanded scale to clearly show individual EPSPs and spikes.
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Figure 9. Responses of MHR neurons and motoneurons to pressing the head. A, Graded presses result in a graded barrage of EPSPs and firing at the highest intensity. This is reversibly blocked by 1 mM kynurenate. B, The excitatory response in MHR neurons reduces when presses are repeated every second. C, The barrage of IPSPs in a ventral, rhythmically active, neuron (VN) also reduces during repeated presses.
To discover if the MHR neurons were directly excited by trigeminal sensory neurons, we investigated their response to electrical stimulation of the cement gland (n = 5) (Fig. 10). In this region of the head there are two types of sensory nerve endings (Roberts, 1980
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Figure 10. Responses of MHRs and ventral spinal neurons (VNs) to electrical stimulation of the cement gland. A, The preparation used. Microelectrodes could record from either MHRs or rostral VNs. Drugs were locally applied via a microperfusion system. B, As stimulus intensity is increased, the short-latency EPSP in an MHR increases in amplitude until a spike is evoked. C, The EPSP in MHRs is blocked by kynurenate. Each trace is an average of eight responses. D, The IPSP in a spinal neuron is blocked by bicuculline. Averages of eight responses. Stimulus indicated by asterisk.
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Figure 11. Latencies of responses of MHRs and VRs to electrical stimulation of the cement gland. A, EPSPs and spikes in an MHR (6 traces overlaid). The latency to the start of the EPSP (arrows) has a smaller variance than the latency to the spike (arrowheads). IPSPs in a ventral spinal neuron (VN) have a long and variable latency (arrows). MHR and VN recorded from two different animals. Stimulus at asterisk. B, Plot of latencies to EPSPs in MHRs and IPSPs in VNs shows the clear difference in timing and variability in delays. Also shown is the delay to the spike in the one MHR in which this could be evoked. Twenty-five latencies were measured in each neuron.
Responses of spinal neurons to activation of the stopping pathway
Because electrical stimulation of the cement gland excited the MHRs and we propose that MHRs inhibit spinal neurons, we also looked at responses to cement gland stimulation in rhythmically active, ventral spinal neurons (presumed motoneurons). In five of six spinal neurons in six separate preparations the response was purely inhibitory (Figs. 10D, 11A) and was fully blocked by bicuculline (Fig. 10D). In one case an excitatory response was also observed at a similar latency. This was presumably because of the activation of fast transient (touch) receptors, but in general it appears that electrical stimulation near the cement gland primarily activated the pressure sensitive afferents.
In each preparation tested, the delay to the start of the IPSPs in ventral neurons was longer and the variation larger than for the EPSPs in MHRs (Fig. 11, Table 1) (mean delay, 12.8 msec ± 1.9 SD; variance, 3.6; n = 25 IPSPs each from six preparations). For individual variances, see Table 1. The latencies of the EPSPs in MHRs and the IPSPs in ventral spinal neurons are compared in Figure 11B. The increased latency and variance for the IPSPs is compatible with a disynaptic pathway from trigeminal sensory neurons, via MHR interneurons (see Discussion).
When the head skin was pressed, ventral spinal neurons that were rhythmically active during swimming received a barrage of IPSPs (n = 8). As has been shown previously (Boothby and Roberts, 1992b
Firing in individual MHRs stops swimming
In seven of nine neurons tested, firing individual MHRs using positive current injection reliably stopped ongoing fictive swimming (Fig. 12). The protocol was to initiate swimming using a brief electrical stimulus to the trunk skin then inject 5-20 positive current pulses 2.4 sec later. This gave rise to between 5 and 40 spikes in the MHR, depending on the amplitude and number of current pulses used. Two MHR neurons had no apparent effect on swimming, however many action potentials were evoked. To assess the number of MHR impulses necessary to stop swimming, the number of MHR impulses that occurred before the last swimming cycle was counted. The number of impulses ranged from 1 to 23 (mean, 4.6 ± 4.4 spikes; n = 7 tadpoles). Without such induced MHR activity, swimming always continued for many seconds before slowing and terminating spontaneously. To quantify this we counted the number of cycles before swimming stopped. Swimming continued for 239 ± 171 cycles (n = 15 responses from 5 tadpoles) with no MHR spikes. After the MHRs were induced to fire swimming then continued for only 2 ± 1 cycles (n = 75 responses from seven tadpoles). In these 75 responses there were 13 in which evoking MHR spikes failed to stop swimming so the stopping effect of MHR spikes was 86% reliable.
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Figure 12. Stimulation of individual MHR neurons can stop ongoing swimming. In three trials in control, swimming (recorded in ventral root, VR) is started using a brief electrical stimulus to the skin (at asterisk). After 2.4 sec five current pulses (solid bar) are injected into the MHR neuron, each resulting in two spikes (inset box shows the end of swimming at a slower time base). This stops swimming on every trial. In bicuculline, firing in the MHR neuron no longer stops swimming (2 trials shown). The second series of current pulses in the MHR neuron consists of 15 pulses, each giving rise to between two and four spikes (inset shows the start of this train). Swimming carried on for at least another 6 sec after end of the trace shown. After 90 sec in wash, activity in the MHR neuron can again stop swimming.
In three experiments the GABAA antagonist bicuculline (20 µM) was applied to the rostral spinal cord. This had no apparent effect on fictive swimming but reversibly blocked the ability of MHR neurons to terminate swimming, even when a larger number of action potentials were evoked (Fig. 12, tested at least six times in each animal). In wash, firing individual MHRs could again reliably stop swimming when tested at least five times in each animal. This shows that the ability of MHRs to stop swimming relies on GABAA-mediated inhibition, as does the normal stopping response (Boothby and Roberts, 1992a
DISCUSSION
Are reticulospinal neurons (MHRs) involved in the natural stopping pathway?
When the head skin is pressed to stop swimming it is known that sensory neurons in the trigeminal are excited to fire action potentials (Roberts and Blight, 1975
Neurons filled in this study share many anatomical features with MHRs (see Results) and can therefore be identified with some confidence as MHRs. Roberts et al. (1987)
The MHRs in this study were excited by pressing the cement gland, as would be expected if the MHRs are involved in the stopping pathway. Boothby and Roberts (1992b)
The best evidence that MHRs are involved in the normal stopping pathway is that firing in individual MHRs could reliably stop swimming. Additionally, the ability of individual MHRs to stop swimming was blocked by bicuculline, showing that it relies on the activation of GABAA receptors. The natural stopping response is also blocked by bicuculline and when the head skin is pressed GABAergic IPSPs are evoked in rhythmic spinal neurons (Boothby and Roberts, 1992b
If most MHRs can stop swimming individually, as a population they must have a very powerful influence on the CPG. This may be to get the very reliable termination of swimming, which is seen when swimming tadpoles bumps into solid objects. Stopping is also very reliable when tested under experimental conditions by pressing on the head skin of tadpoles (80% in restrained tadpoles, 97% in immobilized tadpoles) (Boothby and Roberts 1992a
The source of the midcycle IPSPs seen in MHRs during swimming is likely to be spinal commissural interneurons, which have axons projecting through the hindbrain (Yoshida et al., 1998
Is the stopping pathway disynaptic?
Various possibilities have been put forward to define the stopping pathway in Xenopus, after studies involving various lesions to the CNS (Boothby and Roberts, 1992a
The neuronal pathway that we propose for stopping swimming in Xenopus tadpoles is shown in Figure 13. Trigeminal sensory neurons innervate both the cement gland and the head skin. Slow pressure to either of these leads to multiple action potentials in a number of trigeminal afferent neurons. Their central caudally directed axons project through the hindbrain and release an EAA to excite MHR neurons. If the stimulus is sufficient, one or more MHR neurons will fire action potentials that will propagate into the spinal cord in the caudally directed axons of the MHRs. All MHRs have a commissural axon, but some also have an ipsilateral descending axon, so the action might be bilateral. The axons are presumed to make en passant synapses with neurons that they pass in the caudal hindbrain and spinal cord. At these synapses GABA is released to activate GABAA receptors and terminate swimming activity. Is this simple pathway the only one? The lesion experiments of Boothby and Roberts (1992a)
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Figure 13. The proposed neuronal pathway involved in stopping swimming in Xenopus tadpoles when the head skin is pressed. This schematic diagram shows the nervous system as viewed from above (see Fig. 3). Trigeminal sensory neurons (white) have processes in the skin of the head and cement gland and an axon descending to the caudal hindbrain where synapses are made with MHRs (black). When activated the trigeminal neurons excite the MHRs by releasing an EAA. MHRs all have a contralateral descending axon (solid line), and some have an additional ipsilateral descending axon (dashed line). These axons make en passant synapses with rhythmic spinal neurons (hatching). If the stimulus intensity is sufficient, the MHRs fire action potentials that result in the release of GABA, which activates GABAA receptors and hyperpolarizes the spinal neurons to stop activity in the swimming CPG. Note that Boothby and Roberts (1992a)
Interactions with other sensory pathways
There are four main pathways that can initiate swimming in Xenopus tadpoles (Roberts, 1998
1 and in central axons of 0.15-0.4 msec
These inputs from the pathway that initiates swimming onto neurons involved in stopping swimming mean that the MHRs are a place where the two pathways could interact. Interactions between sensory pathways at the interneuronal level could help to explain some behavioral phenomena such as reduced responsiveness during attachment (discussed above; Lambert and Roberts, 2000
FOOTNOTES Received Jan. 9, 2002; revised March 5, 2002; accepted March 6, 2002.
This work was supported by the Wellcome Trust. We thank Derek Dunn, Julie Hansen, Tim Colburn, and Linda Teagle for technical assistance and Steve Soffe for advice and comments on this manuscript.
Correspondence should be addressed to Prof. Alan Roberts, School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK. E-mail: A.Roberts{at}bristol.ac.uk.
REFERENCES
- Boothby KM, Roberts A (1992a) The stopping response of Xenopus laevis tadpoles: behavior, development and physiology. J Comp Physiol [A] 170:171-180[Medline].
- Boothby KM, Roberts A (1992b) The stopping response of Xenopus laevis tadpoles: pharmacology and intracellular physiology of rhythmic spinal neurones and hindbrain neurones. J Exp Biol 169:65-86
[Abstract/Free Full Text] .- Buchanan JT (2001) Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurobiol 63:441-466[Web of Science][Medline].
- Clarke JDW, Hayes BP, Hunt SP, Roberts A (1984) Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis. J Physiol (Lond) 348:511-525
[Abstract/Free Full Text] .- Dale N, Ottersen OP, Roberts A, Storm-Mathisen J (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255-257[Medline].
- Eaton RC, Lee RKK, Foreman MB (2001) The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63:467-485[Web of Science][Medline].
- Foster RG, Roberts A (1982) the pineal eye in Xenopus laevis embryos and larvae: a photoreceptor with a direct excitatory effect on behavior. J Comp Physiol [A] 145:413-419.
- Fraenkel G (1932) Untersuchungen über die koordination von reflexen und automatisch-nervösen rhythmen bei insekten. I. Die flungreflexe der insecten und ihre koordination. Z Vergl Physiol 16:371-393.
- Gray J, Sand A (1936) The locomotory rhythm of the dogfish. J Exp Biol 13:200-209[Abstract].
- Hayes BP, Roberts A (1983) The anatomy of two functional types of mechanoreceptive "free" nerve ending in the head skin of Xenopus tadpoles. Proc R Soc Lond B Biol Sci 218:61-76[Medline].
- Holstege JC (1991) Ultrastructural evidence for GABAergic brainstem projections to spinal motoneurons in the rat. J Neurosci 11:159-167[Abstract].
- Jamieson D, Roberts A (2000) Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. J Exp Biol 203:1857-1867[Abstract].
- Lambert TD, Roberts A (2000) Tonic activity of trigeminal sensory neurons and reduced responsiveness during cement gland attachment in hatchling Xenopus laevis tadpoles. J Physiol (Lond) 523:272.P.
- Li W-C, Perrins R, Soffe SR, Yoshida M, Walford A, Roberts A (2001) Discriminating classes of spinal interneuron in Xenopus tadpoles. J Comp Neurol 441:248-265[Web of Science][Medline].
- Llinas R, Terzuolo CA (1964) Mechanisms of supraspinal actions upon spinal cord activities. Reticular inhibitory mechanisms on alpha-extensor motoneurons. J Neurophysiol 27:579-591
[Free Full Text] .- Magoun HW, Rhines R (1946) An inhibitory mechanism in the bulbar reticular formation. J Neurophysiol 9:165-171
[Free Full Text] .- Mori S (1987) Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats. Prog Neurobiol 28:161-196[Web of Science][Medline].
- Nieuwkoop PD, Faber J (1956) In: Normal tables of Xenopus laevis (Daudin). Amsterdam: North-Holland.
- Pringle JWS (1974) Locomotion: flight. In: The physiology of the Insecta, Vol 3 (Rockstein M, ed), pp 433-476. London: Academic.
- Roberts A (1975) Mechanisms for the excitation of "free nerve endings". Nature 253:737-738[Medline].
- Roberts A (1978) Pineal eye and behavior in Xenopus tadpoles. Nature 273:774-775[Medline].
- Roberts A (1980) The function and role of two types of mechanoreceptive "free" nerve endings in the head skin of amphibian tadpoles. J Comp Physiol [A] 135:341-348.
- Roberts A (1998) Skin sensory systems of amphibian embryos and young larvae. In: Amphibian biology, Vol 3, "Sensory perception" (Heatwole H, ed), pp 923-935. Chipping Norton, NSW, Australia: Surrey Beatty & Sons.
- Roberts A, Blight AR (1975) Anatomy, physiology and behavioural role of sensory nerve endings in the cement gland of embryonic Xenopus. Proc R Soc Lond B Biol Sci 192:111-127[Medline].
- Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian spinal cord. Philos Trans R Soc Lond B Biol Sci 296:195-212[Medline].
- Roberts A, Sillar KT (1990) Characterization and function of spinal excitatory interneurons with commissural projections in Xenopus laevis tadpoles. Eur J Neurosci 2:1051-1062[Web of Science][Medline].
- Roberts A, Stirling CA (1971) The properties and propagation of a cardiac-like impulse in the skin of young tadpoles. Z Vergl Physiol 71:295-310.
- Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis tadpoles. J Comp Neurol 261:435-449[Web of Science][Medline].
- Roberts A, Soffe SR, Perrins R (1997) Spinal Networks controlling swimming in hatchling Xenopus tadpoles. In: Neurons, networks and motor behavior (Stein PSG, Grillner S, Selverton AI, Stuart DG, eds). Cambridge, MA: MIT.
- Roberts A, Hill NA, Hicks R (2000) Simple mechanisms organise orientation of escape swimming in embryos and hatchling tadpoles of Xenopus laevis. J Exp Biol 203:69-85.
- Satterlie RA, LaBarbera M, Spencer AN (1985) Swimming in the pterpod mollusc, Clione limacina. I. Behavior and morphology. J Exp Biol 166:189-204.
- Sillar KT, Roberts A (1988) A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331:262-265[Medline].
- Sillar KT, Roberts A (1992) Phase-dependent modulation of a cutaneous sensory pathway by glycinergic inhibition from the locomotor rhythm generator in Xenopus embryos. Eur J Neurosci 4:1022-1034[Web of Science][Medline].
- Soffe SR (1990) Active and passive membrane properties of spinal cord neurons which are rhythmically active during swimming in Xenopus embryos. Eur J Neurosci 2:1-10[Web of Science][Medline].
- Soffe SR, Perrins R (1997) Neuronal firing properties and swimming motor patterns in four amphibian embryos: Xenopus, Rana, Bufo and Triturus. J Comp Physiol 181:71-81.
- Stein PSG, Grillner S, Selverston AI, Stuart DG (1997) In: Neurons, networks and motor behavior. Cambridge, MA: MIT.
- Takakusaki K, Kohyama J, Matsuyama K, Mori S (2001) Medullary reticulospinal tract mediating generalised motor inhibition in cats: parallel inhibitory mechanisms acting on motoneurons and on interneuronal transmission in reflex pathways. Neuroscience 103:511-527[Web of Science][Medline].
- van Mier P, ten Donkelaar HJ (1984) Early development of descending pathways from the brain stem to the spinal cord in Xenopus laevis. Anat Embryol 170:295-306[Medline].
- Viana Di Prisco G, Pearlstein E, Le Ray D, Robitaille R, Dubuc R (2000) A cellular mechanism for the transformation of a sensory input into a motor command. J Neurosci 20:8169-8176
[Abstract/Free Full Text] .- Yoshida M, Roberts A, Soffe SR (1998) Axon projections of reciprocal inhibitory interneurons in the spinal cord of young Xenopus tadpoles and implications for the pattern of inhibition during swimming and struggling. J Comp Neurol 400:504-518[Web of Science][Medline].
- Zelenin PV, Grillner S, Orlovsky GN, Deliagina TG (2001) Heterogeniety of the population of command neurons in the lamprey. J Neurosci 21:7793-7803
[Abstract/Free Full Text] .- Zottoli SJ (1978) Comparative morphology of the Mauthner cell in fish and amphibians. In: Neurobiology of the Mauthner cell (Faber DS, Korn H, eds), pp 13-45. New York: Raven.
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