Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input

Yang In Kim, F. E. Dudek

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

1. The electrophysiological properties of suprachiasmatic nucleus (SCN) neurons (n = 33) receiving optic nerve input were studied with intracellular recordings in rat hypothalamic slices maintained in vitro. Our major goal was to provide baseline data concerning the intrinsic membrane properties of these neurons and to test the hypothesis that the neurons are homogeneous electrophysiologically. 2. Action potentials were short in duration and followed by a pronounced hyperpolarizing after-potential. Spike amplitude (58.2 ± 11 mV, mean ± S.E.M.; measured from threshold), spike duration (0.83 ± 0.03 ms; measured at half amplitude) and hyperpolarizing after-potential amplitude (23.9 ± 1.0 mV; measured from threshold) appeared unimodally distributed and did not co-vary. 3. Intracellular injection of depolarizing current pulses evoked spike trains, and spike inactivation, spike broadening and frequency accommodation were always present. An after-hyperpolarization followed the spike train in all but one neuron. 4. Membrane time constant ranged from 7.5 to 21.1 ms (11.4 ± 0.7 ms, n = 27), and its distribution appeared to be unimodal with the peak at ≃10ms. Input resistance ranged from 105 to 626 MΩ (301 ± 23 MΩ, n = 33); the distribution also appeared unimodal with its peak at ~ 250 MΩ. 5. A subpopulation (16 of 33, 48 %) of the neurons exhibited slight (6-29 %) time-dependent inward rectification in their voltage responses to hyperpolarizing current injection. Of the neurons lacking the time-dependent rectification, some (n = 5) exhibited time-independent inward rectification of 6-20 % and others showed no (or < 3%) such rectification. The degree of inward rectification was correlated with neuronal excitability (r = 0.60, P < 0 002; assessed by measuring the steepness of the primary slope of the frequency-current plot) and with the spontaneous firing rate (r=049, P<0007). Furthermore, the neurons with >6% inward rectification (neurons with time-dependent and -independent rectification were combined) were more excitable (362 ± 43 Hz/nA (n = 15) vs. 221 ± 37 Hz/nA (n = 9), P < 0.05) and had a higher spontaneous firing rate (11.1 ± 1.9 Hz (n = 19) vs. 3.9 ± 1.5 Hz (n = 11), P < 0.02) than the neurons with no or negligible (i.e. < 3 %) inward rectification. The two groups, however, were not significantly different in membrane time constant and input resistance. 6. When adequately hyperpolarized, twelve of seventeen (71%) neurons generated small low-threshold spike (LTS) potentials in response to depolarizing current pulses. The neurons with LTS potentials were not significantly different from other neurons (n = 5, 29%) in spontaneous firing rate, excitability, membrane time constant and input resistance. The capacity to generate LTS potentials was not related to the presence of inward rectification. 7. Spontandneous firing (up to 34 Hz) was present in all but six neurons. In general, neurons with a firing rate > 6Hz (71%) had a regular firing pattern, whereas neurons that fired at < 4 Hz (25%) had an irregular firing pattern. Altering the firing rate with intracellular current injection changed the firing pattern. Therefore, depending on the firing rate, and given neuron could show either a regular or an irregular firing pattern. 8. These results suggest that the retinorecipient neurons in the SCN do not form a completely homogeneous group nor clearly distinct classes in terms of intrinsic membrane properties. Furthermore, the data suggest inward rectification may be related to enhanced excitability and firing rate.

Original languageEnglish
Pages (from-to)229-243
Number of pages15
JournalJournal of Physiology
Volume464
Publication statusPublished - 1993 Jan 1
Externally publishedYes

Fingerprint

Suprachiasmatic Nucleus
Optic Nerve
Neurons
Membranes
Injections
Action Potentials

ASJC Scopus subject areas

  • Physiology

Cite this

Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input. / Kim, Yang In; Dudek, F. E.

In: Journal of Physiology, Vol. 464, 01.01.1993, p. 229-243.

Research output: Contribution to journalArticle

@article{6c8eb138692044a78395dc2fdd4e8a14,
title = "Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input",
abstract = "1. The electrophysiological properties of suprachiasmatic nucleus (SCN) neurons (n = 33) receiving optic nerve input were studied with intracellular recordings in rat hypothalamic slices maintained in vitro. Our major goal was to provide baseline data concerning the intrinsic membrane properties of these neurons and to test the hypothesis that the neurons are homogeneous electrophysiologically. 2. Action potentials were short in duration and followed by a pronounced hyperpolarizing after-potential. Spike amplitude (58.2 ± 11 mV, mean ± S.E.M.; measured from threshold), spike duration (0.83 ± 0.03 ms; measured at half amplitude) and hyperpolarizing after-potential amplitude (23.9 ± 1.0 mV; measured from threshold) appeared unimodally distributed and did not co-vary. 3. Intracellular injection of depolarizing current pulses evoked spike trains, and spike inactivation, spike broadening and frequency accommodation were always present. An after-hyperpolarization followed the spike train in all but one neuron. 4. Membrane time constant ranged from 7.5 to 21.1 ms (11.4 ± 0.7 ms, n = 27), and its distribution appeared to be unimodal with the peak at ≃10ms. Input resistance ranged from 105 to 626 MΩ (301 ± 23 MΩ, n = 33); the distribution also appeared unimodal with its peak at ~ 250 MΩ. 5. A subpopulation (16 of 33, 48 {\%}) of the neurons exhibited slight (6-29 {\%}) time-dependent inward rectification in their voltage responses to hyperpolarizing current injection. Of the neurons lacking the time-dependent rectification, some (n = 5) exhibited time-independent inward rectification of 6-20 {\%} and others showed no (or < 3{\%}) such rectification. The degree of inward rectification was correlated with neuronal excitability (r = 0.60, P < 0 002; assessed by measuring the steepness of the primary slope of the frequency-current plot) and with the spontaneous firing rate (r=049, P<0007). Furthermore, the neurons with >6{\%} inward rectification (neurons with time-dependent and -independent rectification were combined) were more excitable (362 ± 43 Hz/nA (n = 15) vs. 221 ± 37 Hz/nA (n = 9), P < 0.05) and had a higher spontaneous firing rate (11.1 ± 1.9 Hz (n = 19) vs. 3.9 ± 1.5 Hz (n = 11), P < 0.02) than the neurons with no or negligible (i.e. < 3 {\%}) inward rectification. The two groups, however, were not significantly different in membrane time constant and input resistance. 6. When adequately hyperpolarized, twelve of seventeen (71{\%}) neurons generated small low-threshold spike (LTS) potentials in response to depolarizing current pulses. The neurons with LTS potentials were not significantly different from other neurons (n = 5, 29{\%}) in spontaneous firing rate, excitability, membrane time constant and input resistance. The capacity to generate LTS potentials was not related to the presence of inward rectification. 7. Spontandneous firing (up to 34 Hz) was present in all but six neurons. In general, neurons with a firing rate > 6Hz (71{\%}) had a regular firing pattern, whereas neurons that fired at < 4 Hz (25{\%}) had an irregular firing pattern. Altering the firing rate with intracellular current injection changed the firing pattern. Therefore, depending on the firing rate, and given neuron could show either a regular or an irregular firing pattern. 8. These results suggest that the retinorecipient neurons in the SCN do not form a completely homogeneous group nor clearly distinct classes in terms of intrinsic membrane properties. Furthermore, the data suggest inward rectification may be related to enhanced excitability and firing rate.",
author = "Kim, {Yang In} and Dudek, {F. E.}",
year = "1993",
month = "1",
day = "1",
language = "English",
volume = "464",
pages = "229--243",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",

}

TY - JOUR

T1 - Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input

AU - Kim, Yang In

AU - Dudek, F. E.

PY - 1993/1/1

Y1 - 1993/1/1

N2 - 1. The electrophysiological properties of suprachiasmatic nucleus (SCN) neurons (n = 33) receiving optic nerve input were studied with intracellular recordings in rat hypothalamic slices maintained in vitro. Our major goal was to provide baseline data concerning the intrinsic membrane properties of these neurons and to test the hypothesis that the neurons are homogeneous electrophysiologically. 2. Action potentials were short in duration and followed by a pronounced hyperpolarizing after-potential. Spike amplitude (58.2 ± 11 mV, mean ± S.E.M.; measured from threshold), spike duration (0.83 ± 0.03 ms; measured at half amplitude) and hyperpolarizing after-potential amplitude (23.9 ± 1.0 mV; measured from threshold) appeared unimodally distributed and did not co-vary. 3. Intracellular injection of depolarizing current pulses evoked spike trains, and spike inactivation, spike broadening and frequency accommodation were always present. An after-hyperpolarization followed the spike train in all but one neuron. 4. Membrane time constant ranged from 7.5 to 21.1 ms (11.4 ± 0.7 ms, n = 27), and its distribution appeared to be unimodal with the peak at ≃10ms. Input resistance ranged from 105 to 626 MΩ (301 ± 23 MΩ, n = 33); the distribution also appeared unimodal with its peak at ~ 250 MΩ. 5. A subpopulation (16 of 33, 48 %) of the neurons exhibited slight (6-29 %) time-dependent inward rectification in their voltage responses to hyperpolarizing current injection. Of the neurons lacking the time-dependent rectification, some (n = 5) exhibited time-independent inward rectification of 6-20 % and others showed no (or < 3%) such rectification. The degree of inward rectification was correlated with neuronal excitability (r = 0.60, P < 0 002; assessed by measuring the steepness of the primary slope of the frequency-current plot) and with the spontaneous firing rate (r=049, P<0007). Furthermore, the neurons with >6% inward rectification (neurons with time-dependent and -independent rectification were combined) were more excitable (362 ± 43 Hz/nA (n = 15) vs. 221 ± 37 Hz/nA (n = 9), P < 0.05) and had a higher spontaneous firing rate (11.1 ± 1.9 Hz (n = 19) vs. 3.9 ± 1.5 Hz (n = 11), P < 0.02) than the neurons with no or negligible (i.e. < 3 %) inward rectification. The two groups, however, were not significantly different in membrane time constant and input resistance. 6. When adequately hyperpolarized, twelve of seventeen (71%) neurons generated small low-threshold spike (LTS) potentials in response to depolarizing current pulses. The neurons with LTS potentials were not significantly different from other neurons (n = 5, 29%) in spontaneous firing rate, excitability, membrane time constant and input resistance. The capacity to generate LTS potentials was not related to the presence of inward rectification. 7. Spontandneous firing (up to 34 Hz) was present in all but six neurons. In general, neurons with a firing rate > 6Hz (71%) had a regular firing pattern, whereas neurons that fired at < 4 Hz (25%) had an irregular firing pattern. Altering the firing rate with intracellular current injection changed the firing pattern. Therefore, depending on the firing rate, and given neuron could show either a regular or an irregular firing pattern. 8. These results suggest that the retinorecipient neurons in the SCN do not form a completely homogeneous group nor clearly distinct classes in terms of intrinsic membrane properties. Furthermore, the data suggest inward rectification may be related to enhanced excitability and firing rate.

AB - 1. The electrophysiological properties of suprachiasmatic nucleus (SCN) neurons (n = 33) receiving optic nerve input were studied with intracellular recordings in rat hypothalamic slices maintained in vitro. Our major goal was to provide baseline data concerning the intrinsic membrane properties of these neurons and to test the hypothesis that the neurons are homogeneous electrophysiologically. 2. Action potentials were short in duration and followed by a pronounced hyperpolarizing after-potential. Spike amplitude (58.2 ± 11 mV, mean ± S.E.M.; measured from threshold), spike duration (0.83 ± 0.03 ms; measured at half amplitude) and hyperpolarizing after-potential amplitude (23.9 ± 1.0 mV; measured from threshold) appeared unimodally distributed and did not co-vary. 3. Intracellular injection of depolarizing current pulses evoked spike trains, and spike inactivation, spike broadening and frequency accommodation were always present. An after-hyperpolarization followed the spike train in all but one neuron. 4. Membrane time constant ranged from 7.5 to 21.1 ms (11.4 ± 0.7 ms, n = 27), and its distribution appeared to be unimodal with the peak at ≃10ms. Input resistance ranged from 105 to 626 MΩ (301 ± 23 MΩ, n = 33); the distribution also appeared unimodal with its peak at ~ 250 MΩ. 5. A subpopulation (16 of 33, 48 %) of the neurons exhibited slight (6-29 %) time-dependent inward rectification in their voltage responses to hyperpolarizing current injection. Of the neurons lacking the time-dependent rectification, some (n = 5) exhibited time-independent inward rectification of 6-20 % and others showed no (or < 3%) such rectification. The degree of inward rectification was correlated with neuronal excitability (r = 0.60, P < 0 002; assessed by measuring the steepness of the primary slope of the frequency-current plot) and with the spontaneous firing rate (r=049, P<0007). Furthermore, the neurons with >6% inward rectification (neurons with time-dependent and -independent rectification were combined) were more excitable (362 ± 43 Hz/nA (n = 15) vs. 221 ± 37 Hz/nA (n = 9), P < 0.05) and had a higher spontaneous firing rate (11.1 ± 1.9 Hz (n = 19) vs. 3.9 ± 1.5 Hz (n = 11), P < 0.02) than the neurons with no or negligible (i.e. < 3 %) inward rectification. The two groups, however, were not significantly different in membrane time constant and input resistance. 6. When adequately hyperpolarized, twelve of seventeen (71%) neurons generated small low-threshold spike (LTS) potentials in response to depolarizing current pulses. The neurons with LTS potentials were not significantly different from other neurons (n = 5, 29%) in spontaneous firing rate, excitability, membrane time constant and input resistance. The capacity to generate LTS potentials was not related to the presence of inward rectification. 7. Spontandneous firing (up to 34 Hz) was present in all but six neurons. In general, neurons with a firing rate > 6Hz (71%) had a regular firing pattern, whereas neurons that fired at < 4 Hz (25%) had an irregular firing pattern. Altering the firing rate with intracellular current injection changed the firing pattern. Therefore, depending on the firing rate, and given neuron could show either a regular or an irregular firing pattern. 8. These results suggest that the retinorecipient neurons in the SCN do not form a completely homogeneous group nor clearly distinct classes in terms of intrinsic membrane properties. Furthermore, the data suggest inward rectification may be related to enhanced excitability and firing rate.

UR - http://www.scopus.com/inward/record.url?scp=0027158420&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0027158420&partnerID=8YFLogxK

M3 - Article

VL - 464

SP - 229

EP - 243

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

ER -