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

Abstract

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

Recording Temperature Affects the Excitability of Mouse Superficial Dorsal Horn Neurons, In Vitro

“…Reduced input resistance at elevated temperature is a consistent finding in a variety of neuronal types (Cao and Oertel 2005;Griffin and Boulant 1995;Klee et al 1974;Lee et al 2005;Thompson et al 1985;Volgushev et al 2000). This is also the case for SDH neurons in general (Table 1); however, when neurons were separated by discharge category the reduction in input resistance was not uniform.…”

“…Extrapolating in vivo functions from data collected at room temperature has proved problematic not only for neuronal excitability (Cao and Oertel 2005;Griffin and Boulant 1995;Lee et al 2005;Thomson et al 1989;Volgushev et al 2000), but also for processes underlying synaptic transmission (Micheva and Smith 2005;Thomson et al 1989;Volgushev et al 2000). Our findings therefore provide a basis for comparing room-temperature recordings with those made at elevated temperature or in vivo.…”

“…In cases where in vitro experiments have been repeated at higher temperatures, many phenomena are markedly different (Cao and Oertel 2005;Lee et al 2005;Micheva and Smith 2005). For example, neurons in the brain stem (Borst and Sakmann 1998;Cao and Oertel 2005), hypothalamus (Griffin and Boulant 1995), hippocampus (Thompson et al 1985), and cortex (Lee et al 2005;Volgushev et al 2000) have altered input resistance, action potential (AP) amplitude, and AP width at elevated temperature (Ն32°C).…”

Transient Receptor Potential Channel Ankyrin-1 Is Not a Cold Sensor for Autonomic Thermoregulation in Rodents

“…But even if there were a central cold sensor for such unusual situations, it probably would not be a TRP channel, as electrophysiological effects of temperature on hypothalamic neurons seem incompatible with mediation by TRP channels (Boulant, 2006). Indeed, several studies have found no difference between temperature-sensitive and insensitive neurons in terms of temperature's effect on resting membrane potentials and currents (Griffin and Boulant, 1995;Zhao and Boulant, 2005).…”

Cellular Mechanisms of Desynchronizing Effects of Hypothermia in an In Vitro Epilepsy Model

“…Previous studies have reported temperature-dependent increases in input resistance [24,25]. The underlying mechanisms of thermal-induced changes in resistance are not very clear, but one intriguing suggestion that still awaits demonstration points at the alteration of membrane structure by temperature [25].…”