Embryonic geniculate ganglion neurons in culture have neurotrophin-specific electrophysiological properties

Neuroscience. 2003;118(1):145-59. doi: 10.1016/s0306-4522(02)00814-x.

Abstract

Geniculate ganglion neurons provide a major source of innervation to mammalian taste organs, including taste buds in the soft palate and in fungiform papillae on the anterior two thirds of the tongue. In and around the fungiform papillae, before taste buds form, neurotrophin mRNAs are expressed in selective spatial and temporal patterns. We hypothesized that neurotrophins would affect electrophysiological properties in embryonic geniculate neurons. Ganglia were explanted from rats at gestational day 16, when growing neurites have entered the papilla core, and maintained in culture with added brain-derived neurotrophic factor (BDNF), neurotrophin 4 (NT4), nerve growth factor (NGF) or neurotrophin 3 (NT3). Neuron survival with BDNF or NT4 was about 80%, whereas with NGF or NT3 less than 15% of neurons survived over 6 days in culture. Whole cell recordings from neurons in ganglion explants with each neurotrophin condition demonstrated distinctive neurophysiological properties related to specific neurotrophins. Geniculate neurons cultured with either BDNF or NT4 had similar passive-membrane and action potential properties, but these characteristics were significantly different from those of neurons cultured with NGF or NT3. NGF-maintained neurons had features of increased excitability including a higher resting membrane potential and a lower current threshold for the action potential. About 70% of neurons produced repetitive action potentials at threshold. Furthermore, compared with neurons cultured with other neurotrophins, a decreased proportion had an inflection on the falling phase of the action potential. NT3-maintained neurons had action potentials that were of relatively large amplitude and short duration, with steep rising and falling slopes. In addition, about 20% responded with a repetitive train of action potentials at threshold. In contrast, with BDNF or NT4 repetitive action potential trains were not observed. The data demonstrate different neurophysiological properties in developing geniculate ganglion neurons maintained with specific neurotrophins. Therefore, we suggest that neurotrophins might influence acquisition of distinctive neurophysiological properties in embryonic geniculate neurons that are fundamental to the formation of peripheral taste circuits and a functioning taste system.

Publication types

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

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Afferent Pathways / drug effects
  • Afferent Pathways / embryology*
  • Afferent Pathways / metabolism
  • Animals
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • Brain-Derived Neurotrophic Factor / pharmacology
  • Cell Differentiation / drug effects
  • Cell Differentiation / physiology*
  • Cells, Cultured
  • Chorda Tympani Nerve / drug effects
  • Chorda Tympani Nerve / embryology
  • Chorda Tympani Nerve / metabolism
  • Female
  • Fetus
  • Geniculate Ganglion / drug effects
  • Geniculate Ganglion / embryology*
  • Geniculate Ganglion / metabolism
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Nerve Growth Factor / genetics
  • Nerve Growth Factor / metabolism
  • Nerve Growth Factor / pharmacology
  • Nerve Growth Factors / genetics
  • Nerve Growth Factors / metabolism*
  • Nerve Growth Factors / pharmacology
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / metabolism*
  • Neurotrophin 3 / genetics
  • Neurotrophin 3 / metabolism
  • Neurotrophin 3 / pharmacology
  • Pregnancy
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Taste / physiology
  • Taste Buds / drug effects
  • Taste Buds / embryology*
  • Taste Buds / metabolism
  • Tongue / cytology
  • Tongue / embryology
  • Tongue / innervation*

Substances

  • Brain-Derived Neurotrophic Factor
  • Nerve Growth Factors
  • Neurotrophin 3
  • RNA, Messenger
  • Nerve Growth Factor
  • neurotrophin 4