Spinal Cord Injury Signiﬁcantly Alters the Properties of Reticulospinal Neurons: I. Biophysical Properties, Firing Patterns, Excitability, and Synaptic Inputs

Cells, 2021 · DOI: https://doi.org/10.3390/cells10081921 · Published: July 29, 2021

Spinal Cord Injury Regenerative Medicine Neurology

Simple Explanation

Following spinal cord injury (SCI) in larval lampreys, the reticulospinal (RS) neurons' axons regenerate, and locomotor function recovers. This study compares the electrophysiological properties of uninjured and injured RS neurons after spinal cord hemi-transections. Injured RS neurons showed changes in firing patterns as early as 2–3 days post-injury, peaking at 2–3 weeks, and returning to normal by 12–16 weeks. These neurons also displayed a hyperpolarized resting membrane potential and altered excitability at 2-3 weeks post-injury. The altered properties observed in injured RS neurons reduced their excitability and spiking frequencies. Researchers found that manipulating the slow afterhyperpolarization (sAHP) did not fully restore normal firing patterns. Sensory-evoked synaptic responses remained largely unaffected after SCI.

Study Duration

2–3 days to 12–16 wks

Participants

Larval sea lampreys (Petromyzon marinus)

Evidence Level

Not specified

Key Findings

1
Changes in firing patterns of injured RS neurons began in as little as 2–3 days following injury, were maximal at ~2–3 weeks, and normal firing patterns were restored by 12–16 weeks.
2
At ~2–3 weeks post-injury, injured RS neurons displayed significant changes including a more hyperpolarized VREST, longer membrane time constant, larger membrane capacitance, altered action potential properties, absence of afterpotential components like sAHP, and reduced firing frequencies.
3
Trigeminal sensory-evoked synaptic responses were not significantly different between uninjured and injured RS neuron pairs, suggesting sensory input remains relatively stable despite injury-induced changes.

Research Summary

Following spinal cord injury (SCI) in larval lampreys, reticulospinal (RS) neurons undergo significant changes in their electrophysiological properties. These changes, termed the 'injury phenotype,' include alterations in firing patterns, membrane properties, action potential characteristics, and excitability. The study reveals that injured RS neurons exhibit reduced excitability and altered firing patterns, which are most pronounced at 2–3 weeks post-injury. These changes are associated with a hyperpolarized resting membrane potential, increased membrane capacitance, and altered action potential thresholds. Despite the observed changes in intrinsic properties, sensory-evoked synaptic responses remain relatively unchanged in injured RS neurons. The findings suggest that SCI induces specific neuronal adaptations that may support axonal regeneration in lampreys.

Practical Implications

Supportive Intracellular Conditions

SCI induces biophysical changes in RS neurons expected to reduce calcium influx, creating supportive conditions for axonal regeneration.

Potential Therapeutic Targets

Understanding these neuronal changes may provide insights for enhancing axonal regeneration following SCI in higher vertebrates, including humans.

Compensatory Mechanisms

Incomplete axonal regeneration can support locomotor recovery due to compensatory mechanisms that facilitate full recovery.

Study Limitations

1
Variations in the degree to which individual neurons respond to SCI.
2
Potential sampling bias due to the death of some Müller cells at longer recovery times.
3
The sAHP was removed or introduced using an injected current waveform to mimic the sAHP rather than using dynamic clamp.

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