Lamina VII neurons are rhythmically active during locomotor-like activity in the neonatal rat spinal cord

MacLean, Jason N.; Hochman, Shawn; Magnuson, David S.K.

doi:10.1016/0304-3940(95)11882-w

Cited by 42 publications

(36 citation statements)

References 27 publications

(20 reference statements)

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“…Similar observations were reported in recent studies in ascending commissural interneurons in the neonatal mouse (Carlin et al 2006;Zhong et al 2006a) and in previous studies in rat spinal interneurons in lamina VII (MacLean et al 1995) and X (Hochman et al 1994a,b). Figure 7 shows a voltage oscillation in a type 3 neuron in lamina X after bath application of 20 M 5-HT.…”

Section: -Ht-induced Membrane Potential Oscillationssupporting

confidence: 91%

“…It was initially suggests that the rat CPG is anatomically localized to the L 1 /L 2 spinal segments (Cazalets et al 1995(Cazalets et al , 1996, but subsequent studies suggest that the hindlimb network is distributed throughout the lumbar and supralumbar spinal cord (Cina and Hochman 2000;Cowley and Schmidt 1997;Kjaerulff et al 1994;Kremer and Lev-Tov 1997;Nishimaru and Kudo 2000;Nishimaru et al 2000;Palmer et al 2001). Early efforts to examine the properties of rodent neurons active during locomotion included intracellular and blind patch recordings MacLean et al 1995), tetrode recordings (Tresch and Kiehn 1999), and calcium imaging (Nakayama et al 2002) from the isolated neonatal rat spinal cord.…”

Section: Introductionmentioning

confidence: 99%

“…We characterize the electrophysiological properties of EGFP-positive neurons ("locomotor neurons") in lamina VII, VIII, and X of T 12 -L 4 segments using whole cell patchclamp techniques. Previous studies demonstrated that 5-HT is necessary and ACh is sufficient to produce locomotor-like activity in isolated spinal cords of neonatal rats and mice (Cowley and Schmidt 1994;Hochman et al 1994a;Jiang et al 1999;Kiehn and Kjaerulff 1996;MacLean et al 1995;Feldman 1986, 1987;Smith et al 1988). Further studies show that several types of 5-HT receptors (5-HT1, 5-HT2, and 5-HT7) are essential in inducing locomotor-like movements in neonatal rat and mouse spinal cord Bracci et al 1998;Cazalets et al 1992Cazalets et al , 1995Hochman et al 2001;Lui and Jordan 2005;Madriaga et al 2004) and in adult rat and mouse transected spinal cord (Landry and Guertin 2004;Landry et al 2006;Ung et al 2008).…”

Section: Introductionmentioning

confidence: 99%

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Electrophysiological and Pharmacological Properties of Locomotor Activity-Related Neurons in cfos-EGFP Mice

Dai

Carlin

Li³

et al. 2009

Journal of Neurophysiology

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Electrophysiological and pharmacological properties of locomotor activityrelated neurons in cfos-EGFP mice. J Neurophysiol 102: 3365-3383, 2009. First published September 30, 2009 doi:10.1152/jn.00265.2009. Although locomotion is known to be generated by networks of spinal neurons, knowledge of the properties of these neurons is limited. Using neonatal transgenic mice that express enhanced green fluorescent protein (EGFP) driven by the c-fos promoter, we visualized EGFPpositive neurons in spinal cord slices from animals that were subjected to a locomotor task or drug cocktail [N-methyl-D-aspartate, serotonin (5-HT), dopamine, and acetylcholine (ACh)]. The activity-dependent expression of EGFP was also induced in dorsal root ganglion neurons with electrical stimulation of the neurons. Following 60 -90 min of swimming, whole cell patch-clamp recordings were made from EGFPϩ neurons in laminae VII, VIII, and X from slices of segments T 12 to L 4 . The EGFPϩ neurons (n ϭ 55) could be classified into three types based on their responses to depolarizing step currents: single spike, phasic firing, and tonic firing. Membrane properties observed in these neurons include hyperpolarization-activated inward currents (29/55), postinhibitory rebound (11/55), and persistent-inward currents (31/55). Bath application of 10 -40 M 5-HT and/or ACh increased neuronal excitability or output with hyperpolarization of voltage threshold and changes in membrane potential. 5-HT also increased input resistance, reduced the afterhyperpolarization (AHP), and induced membrane oscillations, whereas ACh reduced the input resistance and increased the AHP. In this study, we demonstrate a new way of identifying neurons active in locomotion. Our results suggest that the EGFPϩ neurons are a heterogeneous population of interneurons. The actions of 5-HT and ACh on these neurons provide insights into the neuronal properties modulated by these transmitters for generation of locomotion.

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Section: -Ht-induced Membrane Potential Oscillationssupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Electrophysiological and Pharmacological Properties of Locomotor Activity-Related Neurons in cfos-EGFP Mice

Dai

Carlin

Li³

et al. 2009

Journal of Neurophysiology

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“…In agreement with previous work (Menetrey et al, 1985), the number of neurons per segment appeared to decrease with distance from the L5 injection site. Neurons were concentrated in intermediate laminas, especially lamina VII, known to contain locomotor interneurons (Carr et al, 1995;MacLean et al, 1995;Cina and Hochman, 2000;Ahn et al, 2005) (Fig. 8C).…”

Section: Assaymentioning

confidence: 99%

Changes in Motoneuron Properties and Synaptic Inputs Related to Step Training after Spinal Cord Transection in Rats

Petruska¹,

Ichiyama²,

Jindrich³

et al. 2007

J. Neurosci.

138

114

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Although recovery from spinal cord injury is generally meager, evidence suggests that step training can improve stepping performance, particularly after neonatal spinal injury. The location and nature of the changes in neural substrates underlying the behavioral improvements are not well understood. We examined the kinematics of stepping performance and cellular and synaptic electrophysiological parameters in ankle extensor motoneurons in nontrained and treadmill-trained rats, all receiving a complete spinal transection as neonates. For comparison, electrophysiological experiments included animals injured as young adults, which are far less responsive to training. Recovery of treadmill stepping was associated with significant changes in the cellular properties of motoneurons and their synaptic input from spinal white matter [ipsilateral ventrolateral funiculus (VLF)] and muscle spindle afferents. A strong correlation was found between the effectiveness of step training and the amplitude of both the action potential afterhyperpolarization and synaptic inputs to motoneurons (from peripheral nerve and VLF). These changes were absent if step training was unsuccessful, but other spinal projections, apparently inhibitory to step training, became evident. Greater plasticity of axonal projections after neonatal than after adult injury was suggested by anatomical demonstration of denser VLF projections to hindlimb motoneurons after neonatal injury. This finding confirmed electrophysiological measurements and provides a possible mechanism underlying the greater training susceptibility of animals injured as neonates. Thus, we have demonstrated an "age-at-injury"-related difference that may influence training effectiveness, that successful treadmill step training can alter electrophysiological parameters in the transected spinal cord, and that activation of different pathways may prevent functional improvement.

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“…These spinal cord areas contain sufficient neuronal networks for the creation of locomotor rhythms (Kiehn and Kjaerulff 1998;Kjaerulff and Kiehn 1996). Previous studies have shown that many neurons in these areas are rhythmically active during transmitter-induced locomotor activity in the neonatal rat MacLean et al 1995;Raastad et al 1996Raastad et al -1998Tresch and Kiehn 1999). However, the spike numbers and spike timing of interneurons in these regions varies from locomotor cycle to Present address and address for reprint requests: O. Kiehn, Dept.…”

Section: Introductionmentioning

confidence: 99%

Characterization of Reliability of Spike Timing in Spinal Interneurons During Oscillating Inputs

Beierholm

Nielsen

Ryge

et al. 2001

Journal of Neurophysiology

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. Characterization of reliability of spike timing in spinal interneurons during oscillating inputs. J Neurophysiol 86: 1858 -1868, 2001. The spike timing in rhythmically active interneurons in the mammalian spinal locomotor network varies from cycle to cycle. We tested the contribution from passive membrane properties to this variable firing pattern, by measuring the reliability of spike timing, P, in interneurons in the isolated neonatal rat spinal cord, using intracellular injection of sinusoidal command currents of different frequencies (0.325-31.25 Hz). P is a measure of the precision of spike timing. In general, P was low at low frequencies and amplitudes (P ϭ 0 -0.6; 0 -1.875 Hz; 0 -30 pA), and high at high frequencies and amplitudes (P ϭ 0.8 -1; 3.125-31.25 Hz; 30 -200 pA). The exact relationship between P and amplitude was difficult to describe because of the well-known low-pass properties of the membrane, which resulted in amplitude attenuation of high-frequency compared with low-frequency command currents. To formalize the analysis we used a leaky integrate and fire (LIF) model with a noise term added. The LIF model was able to reproduce the experimentally observed properties of P as well as the low-pass properties of the membrane. The LIF model enabled us to use the mathematical theory of nonlinear oscillators to analyze the relationship between amplitude, frequency, and P. This was done by systematically calculating the rotational number, N, defined as the number of spikes divided by the number of periods of the command current, for a large number of frequencies and amplitudes. These calculations led to a phase portrait based on the amplitude of the command current versus the frequency-containing areas [Arnold tongues (ATs)] with the same rotational number. The largest ATs in the phase portrait were those where N was a whole integer, and the largest areas in the ATs were seen for middle to high (Ͼ3 Hz) frequencies and middle to high amplitudes (50 -120 pA). This corresponded to the amplitude-and frequency-evoked increase in P. The model predicted that P would be high when a cell responded with an integer and constant N. This prediction was confirmed by comparing N and P in real experiments. Fitting the result of the LIF model to the experimental data enabled us to estimate the standard deviation of the internal neuronal noise and to use these data to simulate the relationship between N and P in the model. This simulation demonstrated a good correspondence between the theoretical and experimental values. Our data demonstrate that interneurons can respond with a high reliability of spike timing, but only by combining fast and slow oscillations is it possible to obtain a high reliability of firing during rhythmic locomotor movements. Theoretical analysis of the rotation number provided new insights into the mechanism for obtaining reliable spike timing.

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Lamina VII neurons are rhythmically active during locomotor-like activity in the neonatal rat spinal cord

Cited by 42 publications

References 27 publications

Electrophysiological and Pharmacological Properties of Locomotor Activity-Related Neurons in cfos-EGFP Mice

Electrophysiological and Pharmacological Properties of Locomotor Activity-Related Neurons in cfos-EGFP Mice

Changes in Motoneuron Properties and Synaptic Inputs Related to Step Training after Spinal Cord Transection in Rats

Characterization of Reliability of Spike Timing in Spinal Interneurons During Oscillating Inputs

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