scholarly journals Functional characterization of dI6 interneurons in the neonatal mouse spinal cord

2012 ◽  
Vol 107 (12) ◽  
pp. 3256-3266 ◽  
Author(s):  
Jason Dyck ◽  
Guillermo M. Lanuza ◽  
Simon Gosgnach
Keyword(s):  
Spinal Cord ◽  
Action Potentials ◽  
Neural Control ◽  
Motor Behavior ◽  
Functional Characterization ◽  
Rhythmic Activity ◽  
Ventral Root ◽  
Membrane Properties ◽  
Fictive Locomotion ◽  
Transgenic Mouse Line

Our understanding of the neural control of locomotion has been greatly enhanced by the ability to identify and manipulate genetically defined populations of interneurons that comprise the locomotor central pattern generator (CPG). To date, the dI6 interneurons are one of the few populations that settle in the ventral region of the postnatal spinal cord that have not been investigated. In the present study, we utilized a novel transgenic mouse line to electrophysiologically characterize dI6 interneurons located close to the central canal and study their function during fictive locomotion. The majority of dI6 cells investigated were found to be rhythmically active during fictive locomotion and could be divided into two electrophysiologically distinct populations of interneurons. The first population fired rhythmic trains of action potentials that were loosely coupled to ventral root output and contained several intrinsic membrane properties of rhythm-generating neurons, raising the possibility that these cells may be involved in the generation of rhythmic activity in the locomotor CPG. The second population fired rhythmic trains of action potentials that were tightly coupled to ventral root output and lacked intrinsic oscillatory mechanisms, indicating that these neurons may be driven by a rhythm-generating network. Together these results indicate that dI6 neurons comprise an important component of the locomotor CPG that participate in multiple facets of motor behavior.

scholarly journals Commissural Interneurons in Rhythm Generation and Intersegmental Coupling in the Lamprey Spinal Cord

1999 ◽  
Vol 81 (5) ◽  
pp. 2037-2045 ◽  
Author(s):  
James T. Buchanan
Keyword(s):  
Spinal Cord ◽  
Amino Acid ◽  
Excitatory Amino Acid ◽  
Rhythmic Activity ◽  
Ventral Root ◽  
Rhythm Generation ◽  
Spinal Segment ◽  
Spinal Segments ◽  
Autocorrelation Method

Commissural interneurons in rhythm generation and intersegmental coupling in the lamprey spinal cord. To test the necessity of spinal commissural interneurons in the generation of the swim rhythm in lamprey, longitudinal midline cuts of the isolated spinal cord preparation were made. Fictive swimming was then induced by bath perfusion with an excitatory amino acid while recording ventral root activity. When the spinal cord preparation was cut completely along the midline into two lateral hemicords, the rhythmic activity of fictive swimming was lost, usually replaced with continuous ventral root spiking. The loss of the fictive swim rhythm was not due to nonspecific damage produced by the cut because rhythmic activity was present in split regions of spinal cord when the split region was still attached to intact cord. The quality of this persistent rhythmic activity, quantified with an autocorrelation method, declined with the distance of the split spinal segment from the remaining intact spinal cord. The deterioration of the rhythm was characterized by a lengthening of burst durations and a shortening of the interburst silent phases. This pattern of deterioration suggests a loss of rhythmic inhibitory inputs. The same pattern of rhythm deterioration was seen in preparations with the rostral end of the spinal cord cut compared with those with the caudal end cut. The results of this study indicate that commissural interneurons are necessary for the generation of the swimming rhythm in the lamprey spinal cord, and the characteristic loss of the silent interburst phases of the swimming rhythm is consistent with a loss of inhibitory commissural interneurons. The results also suggest that both descending and ascending commissural interneurons are important in the generation of the swimming rhythm. The swim rhythm that persists in the split cord while still attached to an intact portion of spinal cord is thus imposed by interneurons projecting from the intact region of cord into the split region. These projections are functionally short because rhythmic activity was lost within approximately five spinal segments from the intact region of spinal cord.

Activity of commissural interneurons in spinal cord of Xenopus embryos

1984 ◽  
Vol 51 (6) ◽  
pp. 1257-1267 ◽  
Author(s):  
S. R. Soffe ◽  
J. D. Clarke ◽  
A. Roberts
Keyword(s):  
Spinal Cord ◽  
Rhythmic Activity ◽  
Excitatory Input ◽  
Cycle Period ◽  
Fictive Locomotion ◽  
Anatomy And Physiology ◽  
Postsynaptic Potential ◽  
Natural Stimulation ◽  
Xenopus Laevis Embryos ◽  
Stimulation Of

Horseradish peroxidase- (HRP) filled microelectrodes have been used to examine the anatomy and physiology of "commissural interneurons," a morphologically defined class of spinal cord interneuron in Xenopus laevis embryos. Commissural interneurons have unipolar cell bodies in the dorsal half of the spinal cord. Their dendrites lie in the mid to ventral parts of the lateral tracts and their axons cross the cord ventrally, T branch, and ascend and descend on the opposite side of the cord. Recordings were made from animals immobilized in tubocurarine and responding to natural stimulation with three patterns of fictive motor activity. During episodes of fictive swimming, commissural interneurons are phasically excited to fire 1 spike/cycle in phase with motor discharge on the same side and receive a midcycle inhibitory postsynaptic potential (IPSP) in phase with motor discharge on the opposite side. Rhythmic activity is superimposed on a background depolarization. During periods of synchrony, phasic excitatory input doubles in frequency so that cells fire with half the swimming cycle period. The background depolarization is generally stronger than during swimming. During periods of fictive struggling, evoked by electrical stimulation of the skin, commissural interneurons fire a burst of spikes per cycle, cells being relatively hyperpolarized when motoneurons on the opposite side are active. In response to ipsilateral skin stimulation, some cells receive an IPSP at a latency of 12-20 ms. This precedes the onset of fictive locomotion. We discuss how anatomy and activity of commissural interneurons is suitable for a reciprocal inhibitory role.

The Spinal GABAergic System Is a Strong Modulator of Burst Frequency in the Lamprey Locomotor Network

2004 ◽  
Vol 92 (4) ◽  
pp. 2357-2367 ◽  
Author(s):  
David E. Schmitt ◽  
Russell H. Hill ◽  
Sten Grillner
Keyword(s):  
Spinal Cord ◽  
Detailed Analysis ◽  
Gabaergic Neurons ◽  
Ventral Root ◽  
Gabaergic System ◽  
Frequency Regulation ◽  
Fictive Locomotion ◽  
Burst Frequency ◽  
Pronounced Increase ◽  
Spinal Network

The spinal network coordinating locomotion is comprised of a core of glutamate and glycine interneurons. This network is modulated by several transmitter systems including spinal GABA interneurons. The purpose of this study is to explore the contribution of GABAergic neurons to the regulation of locomotor burst frequency in the lamprey model. Using gabazine, a competitive GABAA antagonist more specific than bicuculline, the goal was to provide a detailed analysis of the influence of an endogenous activation of GABAA receptors on fictive locomotion, as well as their possible interaction with GABAB and involvement of GABAC receptors. During N-methyl-d-aspartate (NMDA)-induced fictive locomotion (ventral root recordings in the isolated spinal cord), gabazine (0.1–100 μM) significantly increased the burst rate up to twofold, without changes in regularity or “burst quality.” Gabazine had a proportionately greater effect at higher initial burst rates. Picrotoxin (1–7.5 μM), a less selective GABAA antagonist, also produced a pronounced increase in frequency, but at higher concentrations, the rhythm deteriorated, likely due to the unspecific effects on glycine receptors. The selective GABAB antagonist CGP55845 also increased the frequency, and this effect was markedly enhanced when combined with the GABAA antagonist gabazine. The GABAC antagonist (1,2,5,6-tetrahydropyridine-4-yl)methylphosphinic acid (TPMPA) had no effect on locomotor bursting. Thus the spinal GABA system does play a prominent role in burst frequency regulation in that it reduces the burst frequency by ≤50%, presumably due to presynaptic and soma-dendritic effects documented previously. It is not required for burst generation, but acts as a powerful modulator.

Properties of Rhythmic Activity Generated by the Isolated Spinal Cord of the Neonatal Mouse

2000 ◽  
Vol 84 (6) ◽  
pp. 2821-2833 ◽  
Author(s):  
Patrick Whelan ◽  
Agnes Bonnot ◽  
Michael J. O'Donovan
Keyword(s):  
Spinal Cord ◽  
Ampa Receptors ◽  
Rhythmic Activity ◽  
Ventral Root ◽  
Neonatal Mouse ◽  
Drug Induced ◽  
Lumbosacral Spinal Cord ◽  
Hindlimb Muscle ◽  
Left And Right ◽  
Ventral Roots

We examined the ability of the isolated lumbosacral spinal cord of the neonatal mouse (P0–7) to generate rhythmic motor activity under several different conditions. In the absence of electrical or pharmacological stimulation, we recorded several patterns of spontaneous ventral root depolarization and discharge. Spontaneous, alternating discharge between contralateral ventral roots could occur two to three times over a 10-min interval. We also observed other patterns, including left-right synchrony and rhythmic activity restricted to one side of the cord. Trains of stimuli delivered to the lumbar/coccygeal dorsal roots or the sural nerve reliably evoked episodes of rhythmic activity. During these evoked episodes, rhythmic ventral root discharges could occur on one side of the cord or could alternate from side to side. Bath application of a combination of N-methyl-d,l-aspartate (NMA), serotonin, and dopamine produced rhythmic activity that could last for several hours. Under these conditions, the discharge recorded from the left and right L1–L3 ventral roots alternated. In the L4–L5segments, the discharge had two peaks in each cycle, coincident with discharge of the ipsilateral and contralateral L1–L3 roots. The L6 ventral root discharge alternated with that recorded from the ipsilateral L1–L3 roots. We established that the drug-induced rhythm was locomotor-like by recording an alternating pattern of discharge between ipsilateral flexor and extensor hindlimb muscle nerves. In addition, by recording simultaneously from ventral roots and muscle nerves, we established that ankle flexor discharge was in phase with ipsilateral L1/L2 ventral root discharge, while extensor discharge was in phase with ipsilateral L6 ventral root discharge. Rhythmic patterns of ventral root discharge were preserved following mid-sagittal section of the spinal cord, demonstrating that reciprocal inhibitory connections between the left and right sides of the cord are not essential for rhythmogenesis in the neonatal mouse cord. Blocking N-methyl-d-aspartate receptors, in both the intact and the hemisected preparation, revealed that these receptors contribute to but are not essential for rhythmogenesis. In contrast, the rhythm was abolished following blockade of kainate/AMPA receptors with 6-cyano-7-nitroquinoxalene-2,3-dione. These findings demonstrate that the isolated mouse spinal cord can produce a variety of coordinated activities, including locomotor-like activity. The ability to study these behaviors under a variety of different conditions offers promise for future studies of rhythmogenic mechanisms in this preparation.

scholarly journals Membrane Potential Oscillations in Reticulospinal and Spinobulbar Neurons During Locomotor Activity

2005 ◽  
Vol 94 (1) ◽  
pp. 273-281 ◽  
Author(s):  
James F. Einum ◽  
James T. Buchanan
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Locomotor Activity ◽  
Brain Stem ◽  
Excitatory Amino Acid ◽  
Rhythmic Activity ◽  
Ventral Root ◽  
Potential Oscillations ◽  
Bath Application ◽  
The Brain

Feedback from the spinal locomotor networks provides rhythmic modulation of the membrane potential of reticulospinal (RS) neurons during locomotor activity. To further understand the origins of this rhythmic activity, the timings of the oscillations in spinobulbar (SB) neurons of the spinal cord and in RS neurons of the posterior and middle rhombencephalic reticular nuclei were measured using intracellular microelectrode recordings in the isolated brain stem-spinal cord preparation of the lamprey. A diffusion barrier constructed just caudal to the obex allowed induction of locomotor activity in the spinal cord by bath application of an excitatory amino acid to the spinal bath. All of the ipsilaterally projecting SB neurons recorded had oscillatory membrane potentials with peak depolarizations in phase with the ipsilateral ventral root bursts, whereas the contralaterally projecting SB neurons were about evenly divided between those in phase with the ipsilateral ventral root bursts and those in phase with the contralateral bursts. In the brain stem under these conditions, 75% of RS neurons had peak depolarizations in phase with the ipsilateral ventral root bursts while the remainder had peak depolarizations during the contralateral bursts. Addition of a high-Ca2+, Mg2+ solution to the brain stem bath to reduce polysynaptic activity had little or no effect on oscillation timing in RS neurons, suggesting that direct inputs from SB neurons make a major contribution to RS neuron oscillations under these conditions. Under normal conditions when the brain is participating in the generation of locomotor activity, these spinal inputs will be integrated with other inputs to RS neurons.

scholarly journals How does the Lamprey Central Nervous System make the Lamprey Swim?

1984 ◽  
Vol 112 (1) ◽  
pp. 337-357 ◽  
Author(s):  
STEN GRILLNER ◽  
PETER WALLÉN
Keyword(s):  
Spinal Cord ◽  
Nmda Receptor ◽  
Morphological Characteristics ◽  
Rhythmic Activity ◽  
The Body ◽  
Fictive Locomotion ◽  
Motor Patterns ◽  
Motor Neurones ◽  
Receptor Blockers

The lamprey spinal cord, in isolation or with the brainstem, can be used in vitro. The motor patterns underlying the swimming movements can be elicited by: (1) a pharmacological activation of a specific type of neuronal receptor (NMDA-receptor), that may in other systems give rise to an unstable membrane potential, (2) by stimulation of the brainstem or (3) by tactile activation of skin regions left innervated. In the latter case the initiation of ‘fictive’ swimming is partially caused by a release of a transmitter activating NMDA-receptors, as judged by the effect of NMDA-receptor blockers. The central pattern generator (CPG) is strongly influenced by feedback from mechanosensitive elements, which at least partially reside within the spinal cord. The edge cell in the lamprey spinal cord serves as an intraspinal mechanoreceptor. The ability to generate a coordinated motor output is distributed, since spinal cord sections down to 1.5–2 segments can be made to generate alternating activity. Motor neurones receive an approximately synchronous alternating excitatory and inhibitory drive in each swim cycle and do not appear to be part of the CPG. Motor neurones supplying different parts of the body wall on the same side of a body segment have different morphology with ramifications around different descending axons. The input drive signal during fictive locomotion to motor neurones located close to each other but with different morphological characteristics may differ substantially with regard to the γ-relationship (±25%) and the shape of the oscillation. This implies that even at a segmental level motor neurones may be further subdivided, and furthermore that the ipsilateral network generating the drive signal to ipsilateral motor neurones generates a more complex and individualized output than previously assumed. Motor neurones are not part of the rhythm-generating circuit. The large identifiable interneurones are not required for rhythmic activity to occur although they may be phasically active in the swim cycle. The small segmental interneurones have not yet been completely characterized. Many are phasically active during ‘fictive locomotion’ and lack an apparent axon. Their phase relationships in relation to the burst patterns vary over the entire swim cycle.

Activation of NMDA receptors elecits fictive locomotion and bistable membrane properties in the lamprey spinal cord

1985 ◽  
Vol 336 (2) ◽  
pp. 390-395 ◽  
Author(s):  
K.A. Sigvardt ◽  
S. Grillner ◽  
P. Wallén ◽  
P.A.M. Van Dongen
Keyword(s):  
Spinal Cord ◽  
Nmda Receptors ◽  
Membrane Properties ◽  
Fictive Locomotion

5-HT Modulation of Identified Segmental Premotor Interneurons in the Lamprey Spinal Cord

2006 ◽  
Vol 96 (2) ◽  
pp. 931-935 ◽  
Author(s):  
Zoltán Biró ◽  
Russell H. Hill ◽  
Sten Grillner
Keyword(s):  
Spinal Cord ◽  
Synaptic Transmission ◽  
Membrane Properties ◽  
Frequency Regulation ◽  
Inhibitory Interneurons ◽  
Fictive Locomotion ◽  
Locomotor Rhythm ◽  
Swimming Pattern ◽  
Electrical Component ◽  
Types Of Interneurons

Ipsilaterally projecting spinal excitatory interneurons (EINs) generate the hemisegmental rhythmic locomotor activity in lamprey, while the commissural interneurons ensure proper left-right alternation. 5-HT is a potent modulator of the locomotor rhythm and is endogenously released from the spinal cord during fictive locomotion. The effect of 5-HT was investigated for three segmental premotor interneuron types: EINs, commissural excitatory and commissural inhibitory interneurons. All three types of interneurons produced chemical postsynaptic potentials in motoneurons, but only those from EINs had an electrical component. The effect of 5-HT was studied on the slow afterhyperpolarization, involved in spike frequency regulation, and on the segmental synaptic transmission to motoneurons. 5-HT induced a reduction in the slow afterhyperpolarization and a depression of synaptic transmission in all three types of segmental interneurons. Thus 5-HT is a very potent modulator of membrane properties and synaptic transmission of last-order segmental premotor interneurons. Such modulation of locomotor network interneurons can partially account for the observed effects of 5-HT on the swimming pattern in lamprey.

Induction of action potentials in fish red muscle by denervation

1982 ◽  
Vol 217 (1206) ◽  
pp. 89-99 ◽  
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Neural Control ◽  
Rna Synthesis ◽  
Membrane Resistance ◽  
Membrane Properties ◽  
Sodium Dependent ◽  
Red Muscle ◽  
Miniature Endplate Potentials ◽  
Endplate Potentials

The effects of denervation on the electrical membrane properties of fish red muscle were investigated. Forty to fifty hours after denervation, miniature endplate potentials disappeared abruptly and field stimulation of the nerve within the muscle failed to evoke endplate potentials, indicating that transmission failure occurred at this time. The membrane resistance of the red muscle fibre increased after denervation. Normally innervated fish red muscles do not generate action potentials in response to either nerve or direct muscle stimulation. However, approximately 3 weeks after nerve sectioning, action potentials could be induced in the muscles. The action potential was sodium-dependent, and was sensitive to tetrodotoxin. Actinomycin D injected in the early phase after operation suppressed the induction of the action potential. These results indicate that RNA synthesis is preliminary to the induction of the action potential mechanism, and that this mechanism is under neural control.

Quantitative Investigation of Calcium Signals for Locomotor Pattern Generation in the Lamprey Spinal Cord

2004 ◽  
Vol 92 (3) ◽  
pp. 1796-1806 ◽  
Author(s):  
Gonzalo Viana Di Prisco ◽  
Simon Alford
Keyword(s):  
Spinal Cord ◽  
Ventral Horn ◽  
Pattern Generation ◽  
Membrane Properties ◽  
Fictive Locomotion ◽  
Locomotor Rhythm ◽  
Locomotor Pattern ◽  
Network Coordination ◽  
Neuronal Oscillators ◽  
Intrinsic Membrane Properties

Locomotor pattern generation requires the network coordination of spinal ventral horn neurons acting in concert with the oscillatory properties of individual neurons. In the spinal cord, N-methyl-d-aspartate (NMDA) activates neuronal oscillators that are believed to rely on Ca2+ entry to the cytosol through voltage-operated Ca2+ channels and synaptically activated NMDA receptors. Ca2+ signaling in lamprey ventral horn neurons thus plays a determinant role in the regulation of the intrinsic membrane properties and network synaptic interaction generating spinal locomotor neural pattern activity. We have characterized aspects of this signaling quantitatively for the first time. Resting Ca2+ concentrations were between 87 and 120 nM. Ca2+ concentration measured during fictive locomotion increased from soma to distal dendrites [from 208 ± 27 (SE) nM in the soma to 335 ± 41 nM in the proximal dendrites to 457 ± 68 nM in the distal dendrites]. We sought to determine the temporal and spatial properties of Ca2+ oscillations, imaged with Ca2+-sensitive dyes and correlated with fluctuations in membrane potential, during lamprey fictive locomotion. The Ca2+ signals recorded in the dendrites showed a great deal of spatial heterogeneity. Rapid changes in Ca2+-induced fluorescence coincided with action potentials, which initiated significant Ca2+ transients distributed throughout the neurons. Ca2+ entry to the cytosol coincided with the depolarizing phase of the locomotor rhythm. During fictive locomotion, larger Ca2+ oscillations were recorded in dendrites compared with somata in motoneurons and premotor interneurons. Ca2+ fluctuations were barely detected with dyes of lower affinity providing alternative empirical evidence that Ca2+ responses are limited to hundreds of nanomolars during fictive locomotion.

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