BDNF sensitizes the response of lamina II neurons to high threshold primary afferent inputs

Eur J Neurosci. 2003 Nov;18(9):2467-76. doi: 10.1046/j.1460-9568.2003.02982.x.

Abstract

Brain-derived neurotrophic factor (BDNF) is up-regulated and released in the dorsal horn following peripheral inflammation and has therefore been implicated in spinal mechanisms of sensitization. Despite these observations, the mechanisms associated with such a role for BDNF are not yet fully determined. Here, we investigate the effect of BDNF on dorsal root-evoked synaptic transmission in lamina II neurons. In a transverse spinal cord slice preparation from neonatal rats (P1-15), the whole cell patch-clamp technique was used to record from these neurons. Brief application of BDNF (50-200 ng/mL) facilitated the evoked synaptic currents; they remained enhanced even after BDNF was washed out. A significant minority of cells was minimally affected by BDNF and consistent with this, not all neurons in lamina II were immunoreactive for the tyrosine kinase (trk) B receptor. No facilitation was elicited when N-methyl-d-aspartate (NMDA) receptors were blocked with D-APV, when the postsynaptic NMDA receptors were selectively blocked with intracellular MK-801, or when postsynaptic neurons were loaded with BAPTA. Additionally, inhibiting phospholipase C (PLC) or protein kinase C (PKC) prior to BDNF application completely blocked facilitation. However, once synaptic current underwent BDNF-induced facilitation, the PKC inhibitors failed to reverse the effect, suggesting that PKC is needed for initiation, but not maintenance of BDNF-induced facilitation. These results demonstrate that BDNF functions at the spinal level to enhance synaptic efficacy in an NMDA receptor-dependent manner and requires the action of the PLC/PKC pathway. This action of BDNF may contribute to central sensitization and exaggerated pain states.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • Afferent Pathways / drug effects
  • Afferent Pathways / physiology
  • Animals
  • Animals, Newborn
  • Brain-Derived Neurotrophic Factor / pharmacology
  • Brain-Derived Neurotrophic Factor / physiology*
  • Chelating Agents / pharmacology
  • Dizocilpine Maleate / pharmacology
  • Egtazic Acid / analogs & derivatives*
  • Egtazic Acid / pharmacology
  • Electric Stimulation
  • Electrophysiology
  • Enzyme Inhibitors / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Ganglia, Spinal / physiology*
  • Immunohistochemistry
  • Neurons / chemistry
  • Neurons / drug effects*
  • Neurons / physiology*
  • Patch-Clamp Techniques
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, trkB / analysis
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Spinal Cord / drug effects*
  • Spinal Cord / physiology*
  • Spinal Cord / physiopathology
  • Synaptic Transmission / drug effects*
  • Type C Phospholipases / antagonists & inhibitors
  • Type C Phospholipases / physiology

Substances

  • Brain-Derived Neurotrophic Factor
  • Chelating Agents
  • Enzyme Inhibitors
  • Excitatory Amino Acid Antagonists
  • Receptors, N-Methyl-D-Aspartate
  • Egtazic Acid
  • Dizocilpine Maleate
  • 2-Amino-5-phosphonovalerate
  • Receptor, trkB
  • Protein Kinase C
  • Type C Phospholipases
  • 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid