Intracellular analysis of inherent and synaptic activity in hypothalamic thermosensitive neurones in the rat.

Currás, Margarita C.; Kelso, Stephen R.; Boulant, Jack A.

doi:10.1113/jphysiol.1991.sp018707

Cited by 75 publications

(68 citation statements)

References 14 publications

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“…Regardless of neuronal type, resistance increased with cooling and decreased with warming. Other studies have shown similar thermal effects on the resistances of hypothalamic neurones (Curras et al 1991), hippocampal neurones (Thompson, Masukawa & Prince, 1985) and spinal motoneurones (Pierau, Klee & Klussmann, 1976). Like Fig.…”

Section: Discussionmentioning

confidence: 75%

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Temperature effects on membrane potential and input resistance in rat hypothalamic neurones.

Griffin

Boulant

1995

The Journal of Physiology

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1. Whole-cell recordings were conducted in rat hypothalamic tissue slices to test the hypothesis that thermal changes in membrane potential contribute to neuronal thermosensitivity. Intracellular recordings of membrane potential and input resistance were made in eighty-two neurones, including twenty-four silent neurones and fifty-eight spontaneously firing neurones (22 warm-sensitive neurones and 36 temperature-insensitive neurones). Fifty-seven of the neurones were recorded in the preoptic and anterior hypothalamus. 2. Warm-sensitive neurones increased their firing rates during increases in temperature(1 07 + 0-06 impulses s-' C-1), but their resting membrane potentials were not affected by temperature (0-06 + 0-06 mV C-1). Similarly, temperature did not affect the membrane potentials of temperature-insensitive neurones or silent neurones. 3. Silent neurones had significantly lower input resistances (256-9 + 20-0 MQ), compared with temperature-insensitive (362-6 + 57-2 MQ2) and warm-sensitive neurones (392-2 + 50 0 MQ). Temperature had the same effect on all three types of neurones, such that resistance increased during cooling and decreased during warming. 4. If hyperpolarizing or depolarizing holding currents were applied to neurones, temperature caused changes in the membrane potentials. This spurious effect can be explained by thermally induced changes in the input resistance. 5. Measurements of electrode tip potentials indicated that artificial changes in membrane potential may also be recorded if grounding electrodes are not isolated from the changes in temperature. 6. These results suggest that physiological changes in resting membrane potentials do not determine neuronal warm sensitivity, and thermal changes in input resistance do not determine the primary differences between hypothalamic neurones.Rostral hypothalamic regions, especially the preoptic and anterior hypothalamus (POAH), have been implicated in the regulation of body temperature (Hammel, 1965;Boulant, 1980). Changes in POAH temperature evoke physiological and behavioural thermoregulatory responses, and electrophysiological studies have characterized some hypothalamic neurones as thermosensitive. More than 30% of POAH neurones are warm sensitive, less than 10% are cold sensitive, and the remaining neurones are considered temperature insensitive (Boulant & Dean, 1986). These proportions are similar throughout most of the warm-sensitive and temperature-insensitive diencephalon (Dean & Boulant, 1989). Because warmsensitive hypothalamic neurones also respond to changes in skin and spinal temperatures, they have been viewed as integrators of central and peripheral thermal information (Boulant & Hardy, 1974). In contrast, temperatureinsensitive hypothalamic neurones rarely respond to changes in peripheral temperature, and it has been suggested that they act as reference signals in thermoregulatory neuronal networks (Hammel, 1965). While the mechanism of neuronal thermosensitivity remains controversial, one hypothesis centres on the effect

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Section: Discussionmentioning

confidence: 75%

“…A different theory of neuronal thermosensitivity comes from another intracellular recording study of rat POAH tissue slices (Curras, Kelso & Boulant, 1991 (Purves, 1981), and this appears to be the case in previous studies. …”

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Temperature effects on membrane potential and input resistance in rat hypothalamic neurones.

Griffin

Boulant

1995

The Journal of Physiology

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“…The second, most commonly recognized as truly thermosensitive, is pacemaker-or prepotential-driven, with neurons that fire almost rhythmically as illustrated in Fig. 1A (7,9,15).…”

Section: Resultsmentioning

confidence: 99%

“…It has been suggested that the depolarizing prepotentials which precede an action potential shorten with warming, thus reducing the interspike interval and increasing the firing rate (7,9). An A-type K ϩ current, which regulates the firing rate in other neuronal types, could be responsible for the shortening of the prepotential's duration (9), because it activates and inactivates faster at higher temperatures.…”

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confidence: 99%

Prostaglandin E ₂ -increased thermosensitivity of anterior hypothalamic neurons is associated with depressed inhibition

Tabarean

Behrens

Bartfai

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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Temperature responses of anterior hypothalamic neurons are considered key elements in the regulation of the temperature setpoint of homeotherms. We have investigated the sensitivity to warming of cultured neurons of the AH from mice with electrophysiological and immunocytochemical techniques. In control experiments, only Ϸ9% of the 3-to 5-week-old cells exhibited changes of their basic firing rate when the temperature was raised from 37°C to 40°C. This ratio was increased to 27% after the cultures were ''primed'' by adding prostaglandin E 2 (PGE2), an endogenous pyrogen, in the extracellular medium. In these neurons the firing rate was significantly increased, and the frequency of the gamma ␥-aminobutyric acid (GABA) inhibitory postsynaptic potentials was markedly decreased. In contrast, the resting potential and membrane resistance of the recorded cells remained unchanged. PGE 2 was found to decrease the level of phosphorylation of the extracellular signalregulated kinases 1 and 2 in a subset of GABAergic neurons that express the E-prostanoid receptor type 3. Inhibition of ERK1͞2 by U0126 mimicked the effects of PGE 2. These data indicate that PGE2 acts primarily on the excitability of GABAergic presynaptic cells, most likely via alterations of voltage-gated K ؉ channels. Our results also suggest that far from being an inherent property of a specialized class of neurons, the degree of thermosensitivity can be strongly modulated by synaptic activity and is a more adaptive property of hypothalamic neurons than previously thought. N eurons in the preoptic area (PO) and anterior hypothalamus (AH) are involved in regulating body temperature, as indicated by lesion and thermode implant studies (reviewed in ref. 1). In confirmation, electrophysiological recordings in this region have revealed that some cells, termed warm-sensitive, increase their firing rate when the local temperature is raised. However, numerous complicating factors have hampered their analysis. For example, their definition, which often relies on the increase of the firing rate per°C (impulse s Ϫ1 ͞°C) or is expressed as a Q 10 , varies among authors. Furthermore, their proportion relative to the cold-sensitive and thermo-insensitive neurons is in the rather low range of 20-30% (2-6) with extreme values of 10% (7) to 48% (8), despite the fact that all in vitro studies have been carried out in cells presumed to be highly excitable, because of their unusually high extracellular K ϩ . Another complicating factor is that most hypothalamic warm-sensitive neurons also respond to changes in skin and spinal temperatures (3); therefore, they must be viewed as integrators of thermal information.The mechanism of warm-sensitivity is not fully understood. It has been suggested that the depolarizing prepotentials which precede an action potential shorten with warming, thus reducing the interspike interval and increasing the firing rate (7, 9). An A-type K ϩ current, which regulates the firing rate in other neuronal types, could be responsible for the shortening o...

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“…LTS potentials were identified in a proportion of these cells; however, precise cytoarchitectural sites of recordings were not determined histologically . Another group recently recorded intracellularly from thermosensitive neurons in the medial preoptic area-anterior hypothalamus of the rat (Curras et al 1991). However, the locations of these recordings…”

Section: Introductionmentioning

confidence: 99%

Intracellular Membrane and Synaptic Properties in Medial Preoptic Slices Containing the Sexually Dimorphic Nucleus of the Rat

Hoffman¹,

Kim²,

Gorski³

et al. 1992

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SUMMARY AND CONCLUSIONS 1. Passive and active electrophysiological properties of neurons (n=46) in the medial preoptic area (MPOA) were studied in hypothalamic slices from rats (primarily males). This investigation evaluated whether the MPOA contains a heterogeneous population of cell types, defined on the basis of electrophysiological properties such as low-threshold Ca 2 + spikes (LTS) and current-voltage (I-V) relations. Evoked and spontaneous synaptic potentials were also studied in these neurons. Electrical properties were compared between neurons in the sexually dimorphic nucleus of the preoptic area (SDN-POA) with those situated in other parts of the MPOA.2. Biocytin-injected neurons (n = 24) were found in the SDN-POA, as well as other parts of the medial preoptic nucleus and MPOA. Stained neurons had I or 2 primary dendrites (46% of stained cells) or had multipolar dendritic arrays (54% of cells); dendrites were aspiny or sparsely spiny and displayed limited branching. Morphologically definable cell types were not specific to medial preoptic subdivisions.3. In response to depolarization from a hyperpolarized condition, medial preoptic cells were uniformly capable of generating LTS potentials that generated one or more action potentials. In addition to being voltage dependent, these LTS potentials were time dependent and Ni 2 + sensitive. 5. The typical response to depolarizing current pulses uelivered at or near resting potential was a train of Na + spikes, the frequency of which was directly related to current-pulse intensity. Spike trains displayed moderate spike-frequency adaptation; however, the degree of adaptation was variable across neurons. Afterhyperpolarizations usually followed spike trains.6. Spontaneous postsynaptic potentials (PSPs), most of which were inhibitory, were frequently recorded. In most medial preoptic neurons (83%), extracellular stimulation of the dorsal preoptic region evoked a fast EPSP closely followed by an IPSP. In some neurons, evoked EPSPs were not observed unless the evoked IPSPs were blocked with 10-50 gM bicuculline. The IPSPs reversed at -71 + 5 mV (i.e., near E o _ reported for other hypothalamic neurons).7. These findings indicate that the MPOA is predominantly composed of neurons that, despite having differing morphology, share similar electrophysiological properties. Although electrophysiological properties varied to some extent across neurons, sets of properties did not appear to covary, and thus clearly recognizable cell types were not apparent in this region. The prevalence of such properties as LTS potentials and synaptic inhibition may have relevance for physiological functions associated with this sexually dimorphic region of the hypothalamus.

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Intracellular analysis of inherent and synaptic activity in hypothalamic thermosensitive neurones in the rat.

Cited by 75 publications

References 14 publications

Temperature effects on membrane potential and input resistance in rat hypothalamic neurones.

Temperature effects on membrane potential and input resistance in rat hypothalamic neurones.

Prostaglandin E ₂ -increased thermosensitivity of anterior hypothalamic neurons is associated with depressed inhibition

Intracellular Membrane and Synaptic Properties in Medial Preoptic Slices Containing the Sexually Dimorphic Nucleus of the Rat

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Intracellular analysis of inherent and synaptic activity in hypothalamic thermosensitive neurones in the rat.

Cited by 75 publications

References 14 publications

Temperature effects on membrane potential and input resistance in rat hypothalamic neurones.

Temperature effects on membrane potential and input resistance in rat hypothalamic neurones.

Prostaglandin E 2 -increased thermosensitivity of anterior hypothalamic neurons is associated with depressed inhibition

Intracellular Membrane and Synaptic Properties in Medial Preoptic Slices Containing the Sexually Dimorphic Nucleus of the Rat

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Prostaglandin E ₂ -increased thermosensitivity of anterior hypothalamic neurons is associated with depressed inhibition