Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus

Carolina Gutierrez, Charles L. Cox, John Rinzel, S. Murray Sherman

Research output: Contribution to journalArticle

Abstract

The low-threshold spike (LTS), generated by the transient Ca2+ current /T, plays a pivotal role in thalamic relay cell responsiveness and thus in the nature of the thalamic relay. By injecting depolarizing current ramps at various rates to manipulate the slope of membrane depolarization (dV/dt), we found that an LTS occurred only if dV/dt exceeded a minimum value of ∼5-12 mV/sec. We injected current ramps of variable dV/dt into relay cells that were sufficiently hyperpolarized to de-inactivate /T completely. Higher values of dV/dt activated an LTS. However, lower values of dV/dt eventually led to tonic firing without ever activating an LTS; apparently, the inactivation of /T proceeded before /T could be recruited. Because the maximum rate of rise of the LTS decreased with slower activating ramps of injected current, we conclude that slower ramps allow increasing inactivation of /T before the threshold for its activation gating is reached, and when the injected ramps have a sufficiently low dV/dt, the inactivation is severe enough to prevent activation of an LTS. In the presence of Cs+, we found that even the lowest dV/dt that we applied led to LTS activation, apparently because Cs+ reduced the K+ "leak" conductance and increased neuronal input resistance. Nonetheless, under normal conditions, our data suggest that there is neither significant window current (related to the overlap of the inactivation and activation curves for /T), rhythmogenic properties, nor bistability properties for these neurons. Our theoretical results using a minimal model of LTS excitability in these neurons are consistent with the experimental observations and support our conclusions. We suggest that inputs activating very slow EPSPs (i.e., via metabotropic receptors) may be able to inactivate/T without generating sizable/T and a spurious burst of action potentials to cortex.

Original languageEnglish (US)
Pages (from-to)1022-1032
Number of pages11
JournalJournal of Neuroscience
Volume21
Issue number3
StatePublished - 2001

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Geniculate Bodies
Architectural Accessibility
Cats
Neurons
Excitatory Postsynaptic Potentials
Action Potentials
Membranes

Keywords

  • Burst firing
  • Lateral geniculate nucleus
  • Low-threshold spike
  • T channel
  • Thalamus
  • Window current

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus. / Gutierrez, Carolina; Cox, Charles L.; Rinzel, John; Sherman, S. Murray.

In: Journal of Neuroscience, Vol. 21, No. 3, 2001, p. 1022-1032.

Research output: Contribution to journalArticle

Gutierrez, Carolina ; Cox, Charles L. ; Rinzel, John ; Sherman, S. Murray. / Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus. In: Journal of Neuroscience. 2001 ; Vol. 21, No. 3. pp. 1022-1032.
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AB - The low-threshold spike (LTS), generated by the transient Ca2+ current /T, plays a pivotal role in thalamic relay cell responsiveness and thus in the nature of the thalamic relay. By injecting depolarizing current ramps at various rates to manipulate the slope of membrane depolarization (dV/dt), we found that an LTS occurred only if dV/dt exceeded a minimum value of ∼5-12 mV/sec. We injected current ramps of variable dV/dt into relay cells that were sufficiently hyperpolarized to de-inactivate /T completely. Higher values of dV/dt activated an LTS. However, lower values of dV/dt eventually led to tonic firing without ever activating an LTS; apparently, the inactivation of /T proceeded before /T could be recruited. Because the maximum rate of rise of the LTS decreased with slower activating ramps of injected current, we conclude that slower ramps allow increasing inactivation of /T before the threshold for its activation gating is reached, and when the injected ramps have a sufficiently low dV/dt, the inactivation is severe enough to prevent activation of an LTS. In the presence of Cs+, we found that even the lowest dV/dt that we applied led to LTS activation, apparently because Cs+ reduced the K+ "leak" conductance and increased neuronal input resistance. Nonetheless, under normal conditions, our data suggest that there is neither significant window current (related to the overlap of the inactivation and activation curves for /T), rhythmogenic properties, nor bistability properties for these neurons. Our theoretical results using a minimal model of LTS excitability in these neurons are consistent with the experimental observations and support our conclusions. We suggest that inputs activating very slow EPSPs (i.e., via metabotropic receptors) may be able to inactivate/T without generating sizable/T and a spurious burst of action potentials to cortex.

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