Intermediate gray matter interneurons in the lumbar spinal cord play a critical and necessary role in coordinated locomotion

PLoS One. 2023 Oct 31;18(10):e0291740. doi: 10.1371/journal.pone.0291740. eCollection 2023.

Abstract

Locomotion is a complex task involving excitatory and inhibitory circuitry in spinal gray matter. While genetic knockouts examine the function of individual spinal interneuron (SpIN) subtypes, the phenotype of combined SpIN loss remains to be explored. We modified a kainic acid lesion to damage intermediate gray matter (laminae V-VIII) in the lumbar spinal enlargement (spinal L2-L4) in female rats. A thorough, tailored behavioral evaluation revealed deficits in gross hindlimb function, skilled walking, coordination, balance and gait two weeks post-injury. Using a Random Forest algorithm, we combined these behavioral assessments into a highly predictive binary classification system that strongly correlated with structural deficits in the rostro-caudal axis. Machine-learning quantification confirmed interneuronal damage to laminae V-VIII in spinal L2-L4 correlates with hindlimb dysfunction. White matter alterations and lower motoneuron loss were not observed with this KA lesion. Animals did not regain lost sensorimotor function three months after injury, indicating that natural recovery mechanisms of the spinal cord cannot compensate for loss of laminae V-VIII neurons. As gray matter damage accounts for neurological/walking dysfunction in instances of spinal cord injury affecting the cervical or lumbar enlargement, this research lays the groundwork for new neuroregenerative therapies to replace these lost neuronal pools vital to sensorimotor function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Gray Matter* / pathology
  • Interneurons / physiology
  • Locomotion / physiology
  • Motor Neurons / physiology
  • Rats
  • Spinal Cord / pathology
  • Spinal Cord Injuries*

Grants and funding

Deutsche Forschungsgemeinschaft (DFG):Radhika Puttagunta PU 425/4-3; Deutsche Forschungsgemeinschaft (DFG):Norbert Weidner WE 2165/4-3; Deutsche Forschungsgemeinschaft (DFG):Radhika Puttagunta SFB1158 A06; Deutsche Forschungsgemeinschaft (DFG):Norbert Weidner SFB1158 A06; Olympia Morata Program Fellowship of the University of Heidelberg Faculty of Medicine:Radhika Puttagunta.