Two kinetically distinct components of hyperpolarization-activated current in rat superior colliculus-projecting neurons

Joel Solomon, J. M. Nerbonne

Research output: Contribution to journalArticle

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Abstract

1. Whole-cell and perforated patch recording techniques were used to examine the activation, deactivation and inactivation of the time-dependent hyperpolarization-activated inward currents (I(h)) in isolated superior colliculus-projecting (SCP) neurons from rat primary visual cortex. 2. Examination of inward current waveforms revealed the presence of two kinetically distinct components of I(h):one that activates with a time constant of the order of hundreds of milliseconds, and one that activates with a time constant of the order of seconds. We have termed these I(h,f) and I(h,s), to denote the fast and slow components, respectively, of current activation. The time constants of activation of both I(h,f) and I(h,s) decrease with increasing membrane hyperpolarization. 3. Following the onset of hyperpolarizing voltage steps, a delay is evident prior to time-dependent inward current activation. This delay is voltage dependent and decreases with increasing membrane hyperpolarization. 4. The sigmoidal inward current waveforms are well fitted by the sum of two exponentials in which the faster term, corresponding to the activation of I(h,f), is raised to the power 1.34 ± 0.26 (mean ± S.D.). The non-integral exponent suggests that I(h,f) activation involves at least two energetically non-equivalent gating transitions prior to channel opening. 5. Over a limited voltage range, tail currents could also be resolved into two distinct components. The faster component, which corresponds to the deactivation of I(h,f), decayed over a single exponential time course with a mean (± S.D.) time constant of 355 ± 161 ms at -70 mV. I(h,s) decay also followed a single exponential time course with a mean (± S.D.) time constant of 2428 ± 1285 ms at -70 mV. Both deactivation time constants decreased with increasing depolarization. 6. The separation of inward current activation and deactivation into two distinct components and the lack of correlation between the relative amplitudes of these components suggest that I(h,f) and I(h,s) reflect the presence of two functionally distinct channel populations. 7. No decrements in time-dependent hyperpolarization-activated inward currents were observed during hyperpolarizations lasting up to 18 s, suggesting that neither I(h,f) nor I(h,s) inactivates from the open state. In addition, 10 s depolarizations to 0 mV prior to activation did not alter the waveforms of the inward currents activated directly from -40 mV, suggesting that I(h,f) and I(h,s) also do not inactivate from closed states. 8. The hyperpolarization-activated currents in rat SCP neurons are ideally suited to contribute to the control of the resting membrane potential and input resistance. Furthermore, the time-dependent properties of I(h,f) and I(h,s) may lead to the generation of complex firing patterns such as the rebound firing of action potentials following synaptic inhibition, as well as contribute to the generation and maintenance of rhythmic firing.

Original languageEnglish (US)
Pages (from-to)291-313
Number of pages23
JournalJournal of Physiology
Volume469
StatePublished - 1993
Externally publishedYes

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Superior Colliculi
Neurons
Membranes
Visual Cortex
Membrane Potentials
Action Potentials
Tail
Maintenance

ASJC Scopus subject areas

  • Physiology

Cite this

Two kinetically distinct components of hyperpolarization-activated current in rat superior colliculus-projecting neurons. / Solomon, Joel; Nerbonne, J. M.

In: Journal of Physiology, Vol. 469, 1993, p. 291-313.

Research output: Contribution to journalArticle

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N2 - 1. Whole-cell and perforated patch recording techniques were used to examine the activation, deactivation and inactivation of the time-dependent hyperpolarization-activated inward currents (I(h)) in isolated superior colliculus-projecting (SCP) neurons from rat primary visual cortex. 2. Examination of inward current waveforms revealed the presence of two kinetically distinct components of I(h):one that activates with a time constant of the order of hundreds of milliseconds, and one that activates with a time constant of the order of seconds. We have termed these I(h,f) and I(h,s), to denote the fast and slow components, respectively, of current activation. The time constants of activation of both I(h,f) and I(h,s) decrease with increasing membrane hyperpolarization. 3. Following the onset of hyperpolarizing voltage steps, a delay is evident prior to time-dependent inward current activation. This delay is voltage dependent and decreases with increasing membrane hyperpolarization. 4. The sigmoidal inward current waveforms are well fitted by the sum of two exponentials in which the faster term, corresponding to the activation of I(h,f), is raised to the power 1.34 ± 0.26 (mean ± S.D.). The non-integral exponent suggests that I(h,f) activation involves at least two energetically non-equivalent gating transitions prior to channel opening. 5. Over a limited voltage range, tail currents could also be resolved into two distinct components. The faster component, which corresponds to the deactivation of I(h,f), decayed over a single exponential time course with a mean (± S.D.) time constant of 355 ± 161 ms at -70 mV. I(h,s) decay also followed a single exponential time course with a mean (± S.D.) time constant of 2428 ± 1285 ms at -70 mV. Both deactivation time constants decreased with increasing depolarization. 6. The separation of inward current activation and deactivation into two distinct components and the lack of correlation between the relative amplitudes of these components suggest that I(h,f) and I(h,s) reflect the presence of two functionally distinct channel populations. 7. No decrements in time-dependent hyperpolarization-activated inward currents were observed during hyperpolarizations lasting up to 18 s, suggesting that neither I(h,f) nor I(h,s) inactivates from the open state. In addition, 10 s depolarizations to 0 mV prior to activation did not alter the waveforms of the inward currents activated directly from -40 mV, suggesting that I(h,f) and I(h,s) also do not inactivate from closed states. 8. The hyperpolarization-activated currents in rat SCP neurons are ideally suited to contribute to the control of the resting membrane potential and input resistance. Furthermore, the time-dependent properties of I(h,f) and I(h,s) may lead to the generation of complex firing patterns such as the rebound firing of action potentials following synaptic inhibition, as well as contribute to the generation and maintenance of rhythmic firing.

AB - 1. Whole-cell and perforated patch recording techniques were used to examine the activation, deactivation and inactivation of the time-dependent hyperpolarization-activated inward currents (I(h)) in isolated superior colliculus-projecting (SCP) neurons from rat primary visual cortex. 2. Examination of inward current waveforms revealed the presence of two kinetically distinct components of I(h):one that activates with a time constant of the order of hundreds of milliseconds, and one that activates with a time constant of the order of seconds. We have termed these I(h,f) and I(h,s), to denote the fast and slow components, respectively, of current activation. The time constants of activation of both I(h,f) and I(h,s) decrease with increasing membrane hyperpolarization. 3. Following the onset of hyperpolarizing voltage steps, a delay is evident prior to time-dependent inward current activation. This delay is voltage dependent and decreases with increasing membrane hyperpolarization. 4. The sigmoidal inward current waveforms are well fitted by the sum of two exponentials in which the faster term, corresponding to the activation of I(h,f), is raised to the power 1.34 ± 0.26 (mean ± S.D.). The non-integral exponent suggests that I(h,f) activation involves at least two energetically non-equivalent gating transitions prior to channel opening. 5. Over a limited voltage range, tail currents could also be resolved into two distinct components. The faster component, which corresponds to the deactivation of I(h,f), decayed over a single exponential time course with a mean (± S.D.) time constant of 355 ± 161 ms at -70 mV. I(h,s) decay also followed a single exponential time course with a mean (± S.D.) time constant of 2428 ± 1285 ms at -70 mV. Both deactivation time constants decreased with increasing depolarization. 6. The separation of inward current activation and deactivation into two distinct components and the lack of correlation between the relative amplitudes of these components suggest that I(h,f) and I(h,s) reflect the presence of two functionally distinct channel populations. 7. No decrements in time-dependent hyperpolarization-activated inward currents were observed during hyperpolarizations lasting up to 18 s, suggesting that neither I(h,f) nor I(h,s) inactivates from the open state. In addition, 10 s depolarizations to 0 mV prior to activation did not alter the waveforms of the inward currents activated directly from -40 mV, suggesting that I(h,f) and I(h,s) also do not inactivate from closed states. 8. The hyperpolarization-activated currents in rat SCP neurons are ideally suited to contribute to the control of the resting membrane potential and input resistance. Furthermore, the time-dependent properties of I(h,f) and I(h,s) may lead to the generation of complex firing patterns such as the rebound firing of action potentials following synaptic inhibition, as well as contribute to the generation and maintenance of rhythmic firing.

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