Electrophysiology of guinea-pig supraoptic neurones: Role of a hyperpolarization-activated cation current in phasic firing

Research output: Contribution to journalArticle

46 Citations (Scopus)

Abstract

1. Immunocytochemically identified magnocellular neurosecretory cells (MNCs) in the guinea-pig supraoptic nucleus (SON) were studied using the in vitro intracellular recording technique. Cells were identified as containing arginine vasopressin (AVP) or oxytocin (OT) following recordings made with biocytin-filled electrodes. Both AVP and OT MNCs demonstrated a fusiform or pyramidal shape (15-20 μm by 26-39 μm), with two to three processes. There were no significant differences in the proportion of AVP and OT cells in the retrochiasmatic (caudal) versus the rostral slices. 2. No significant differences in passive membrane properties were observed between AVP and OT cells, except that AVP cells exhibited a significantly broader action potential width (1.51 ± 0.1 ms, n = 11) than did OT cells (1.01 ± 0.08 ms, n = 7). 3. Firing patterns were recorded for 100 MNCs, 41% of which fired in a phasic manner (repeated clustering of action potentials into bursts). Of the seventy-seven cells which were immunocytochemically identified, only AVP-containing MNCs displayed phasic firing. Phasic firing occurred only in MNCs demonstrating a depolarizing potential which followed hyperpolarizing after-potentials (HAPs). The presence of the depolarizing potential was not always associated with phasic firing, however, as both OT cells and non-phasic AVP cells sometimes exhibited a depolarizing potential. 4. In 160 MNCs examined for the presence of the time-dependent inward rectification (TDR in current clamp, or I(h) in voltage clamp), a significant difference in the proportion of cells expressing the I(h) was observed in the two cell types. The was expressed in forty-five of fifty-four AVP MNCs (83%) and in six of fifteen OT MNCs (40%). No significant association was found with firing pattern. 5. The I(h) exhibited properties similar to those found in other CNS and peripheral tissues. It appeared on steps to potentials more hyperpolarized than -65 mV. It was augmented by raising the extracellular potassium concentration, blocked by 2 mM CsCl, and insensitive to 100-500 μM BaCl2. Activation followed a single exponential, and the time constant of activation was voltage dependent. 6. The adenylate cyclase activator forskolin increased the I(h) and shifted its activation curve to more depolarized levels. In cells recorded for several hours, the I(h) varied in amplitude, suggesting intrinsic modulation, possibly by intracellular second messenger systems. The I(h) in guinea-pig SON MNCs appears to serve an excitatory role, bringing cells closer to firing threshold.

Original languageEnglish (US)
Pages (from-to)407-425
Number of pages19
JournalJournal of Physiology
Volume460
StatePublished - 1993

Fingerprint

Electrophysiology
Cations
Guinea Pigs
Neurons
Arginine Vasopressin
Vasotocin
Oxytocin
Supraoptic Nucleus
Second Messenger Systems
Action Potentials

ASJC Scopus subject areas

  • Physiology

Cite this

@article{2075e9cb105446fc9df89129c1e2ddea,
title = "Electrophysiology of guinea-pig supraoptic neurones: Role of a hyperpolarization-activated cation current in phasic firing",
abstract = "1. Immunocytochemically identified magnocellular neurosecretory cells (MNCs) in the guinea-pig supraoptic nucleus (SON) were studied using the in vitro intracellular recording technique. Cells were identified as containing arginine vasopressin (AVP) or oxytocin (OT) following recordings made with biocytin-filled electrodes. Both AVP and OT MNCs demonstrated a fusiform or pyramidal shape (15-20 μm by 26-39 μm), with two to three processes. There were no significant differences in the proportion of AVP and OT cells in the retrochiasmatic (caudal) versus the rostral slices. 2. No significant differences in passive membrane properties were observed between AVP and OT cells, except that AVP cells exhibited a significantly broader action potential width (1.51 ± 0.1 ms, n = 11) than did OT cells (1.01 ± 0.08 ms, n = 7). 3. Firing patterns were recorded for 100 MNCs, 41{\%} of which fired in a phasic manner (repeated clustering of action potentials into bursts). Of the seventy-seven cells which were immunocytochemically identified, only AVP-containing MNCs displayed phasic firing. Phasic firing occurred only in MNCs demonstrating a depolarizing potential which followed hyperpolarizing after-potentials (HAPs). The presence of the depolarizing potential was not always associated with phasic firing, however, as both OT cells and non-phasic AVP cells sometimes exhibited a depolarizing potential. 4. In 160 MNCs examined for the presence of the time-dependent inward rectification (TDR in current clamp, or I(h) in voltage clamp), a significant difference in the proportion of cells expressing the I(h) was observed in the two cell types. The was expressed in forty-five of fifty-four AVP MNCs (83{\%}) and in six of fifteen OT MNCs (40{\%}). No significant association was found with firing pattern. 5. The I(h) exhibited properties similar to those found in other CNS and peripheral tissues. It appeared on steps to potentials more hyperpolarized than -65 mV. It was augmented by raising the extracellular potassium concentration, blocked by 2 mM CsCl, and insensitive to 100-500 μM BaCl2. Activation followed a single exponential, and the time constant of activation was voltage dependent. 6. The adenylate cyclase activator forskolin increased the I(h) and shifted its activation curve to more depolarized levels. In cells recorded for several hours, the I(h) varied in amplitude, suggesting intrinsic modulation, possibly by intracellular second messenger systems. The I(h) in guinea-pig SON MNCs appears to serve an excitatory role, bringing cells closer to firing threshold.",
author = "Erickson, {K. R.} and Oline Ronnekleiv and Martin Kelly",
year = "1993",
language = "English (US)",
volume = "460",
pages = "407--425",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",

}

TY - JOUR

T1 - Electrophysiology of guinea-pig supraoptic neurones

T2 - Role of a hyperpolarization-activated cation current in phasic firing

AU - Erickson, K. R.

AU - Ronnekleiv, Oline

AU - Kelly, Martin

PY - 1993

Y1 - 1993

N2 - 1. Immunocytochemically identified magnocellular neurosecretory cells (MNCs) in the guinea-pig supraoptic nucleus (SON) were studied using the in vitro intracellular recording technique. Cells were identified as containing arginine vasopressin (AVP) or oxytocin (OT) following recordings made with biocytin-filled electrodes. Both AVP and OT MNCs demonstrated a fusiform or pyramidal shape (15-20 μm by 26-39 μm), with two to three processes. There were no significant differences in the proportion of AVP and OT cells in the retrochiasmatic (caudal) versus the rostral slices. 2. No significant differences in passive membrane properties were observed between AVP and OT cells, except that AVP cells exhibited a significantly broader action potential width (1.51 ± 0.1 ms, n = 11) than did OT cells (1.01 ± 0.08 ms, n = 7). 3. Firing patterns were recorded for 100 MNCs, 41% of which fired in a phasic manner (repeated clustering of action potentials into bursts). Of the seventy-seven cells which were immunocytochemically identified, only AVP-containing MNCs displayed phasic firing. Phasic firing occurred only in MNCs demonstrating a depolarizing potential which followed hyperpolarizing after-potentials (HAPs). The presence of the depolarizing potential was not always associated with phasic firing, however, as both OT cells and non-phasic AVP cells sometimes exhibited a depolarizing potential. 4. In 160 MNCs examined for the presence of the time-dependent inward rectification (TDR in current clamp, or I(h) in voltage clamp), a significant difference in the proportion of cells expressing the I(h) was observed in the two cell types. The was expressed in forty-five of fifty-four AVP MNCs (83%) and in six of fifteen OT MNCs (40%). No significant association was found with firing pattern. 5. The I(h) exhibited properties similar to those found in other CNS and peripheral tissues. It appeared on steps to potentials more hyperpolarized than -65 mV. It was augmented by raising the extracellular potassium concentration, blocked by 2 mM CsCl, and insensitive to 100-500 μM BaCl2. Activation followed a single exponential, and the time constant of activation was voltage dependent. 6. The adenylate cyclase activator forskolin increased the I(h) and shifted its activation curve to more depolarized levels. In cells recorded for several hours, the I(h) varied in amplitude, suggesting intrinsic modulation, possibly by intracellular second messenger systems. The I(h) in guinea-pig SON MNCs appears to serve an excitatory role, bringing cells closer to firing threshold.

AB - 1. Immunocytochemically identified magnocellular neurosecretory cells (MNCs) in the guinea-pig supraoptic nucleus (SON) were studied using the in vitro intracellular recording technique. Cells were identified as containing arginine vasopressin (AVP) or oxytocin (OT) following recordings made with biocytin-filled electrodes. Both AVP and OT MNCs demonstrated a fusiform or pyramidal shape (15-20 μm by 26-39 μm), with two to three processes. There were no significant differences in the proportion of AVP and OT cells in the retrochiasmatic (caudal) versus the rostral slices. 2. No significant differences in passive membrane properties were observed between AVP and OT cells, except that AVP cells exhibited a significantly broader action potential width (1.51 ± 0.1 ms, n = 11) than did OT cells (1.01 ± 0.08 ms, n = 7). 3. Firing patterns were recorded for 100 MNCs, 41% of which fired in a phasic manner (repeated clustering of action potentials into bursts). Of the seventy-seven cells which were immunocytochemically identified, only AVP-containing MNCs displayed phasic firing. Phasic firing occurred only in MNCs demonstrating a depolarizing potential which followed hyperpolarizing after-potentials (HAPs). The presence of the depolarizing potential was not always associated with phasic firing, however, as both OT cells and non-phasic AVP cells sometimes exhibited a depolarizing potential. 4. In 160 MNCs examined for the presence of the time-dependent inward rectification (TDR in current clamp, or I(h) in voltage clamp), a significant difference in the proportion of cells expressing the I(h) was observed in the two cell types. The was expressed in forty-five of fifty-four AVP MNCs (83%) and in six of fifteen OT MNCs (40%). No significant association was found with firing pattern. 5. The I(h) exhibited properties similar to those found in other CNS and peripheral tissues. It appeared on steps to potentials more hyperpolarized than -65 mV. It was augmented by raising the extracellular potassium concentration, blocked by 2 mM CsCl, and insensitive to 100-500 μM BaCl2. Activation followed a single exponential, and the time constant of activation was voltage dependent. 6. The adenylate cyclase activator forskolin increased the I(h) and shifted its activation curve to more depolarized levels. In cells recorded for several hours, the I(h) varied in amplitude, suggesting intrinsic modulation, possibly by intracellular second messenger systems. The I(h) in guinea-pig SON MNCs appears to serve an excitatory role, bringing cells closer to firing threshold.

UR - http://www.scopus.com/inward/record.url?scp=0027459492&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0027459492&partnerID=8YFLogxK

M3 - Article

C2 - 8487202

AN - SCOPUS:0027459492

VL - 460

SP - 407

EP - 425

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

ER -