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Hypothalamic Neurons Regulating Body Temperature

Jack A. Boulant

10.1002/cphy.cp040106

Source: Supplement 14: Handbook of Physiology, Environmental Physiology

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Types of Neurons
1.1 Criteria for Neuronal Thermosensitivity
1.2 Distribution of Thermosensitive Neurons
2 Mechanisms of Neuronal Thermosensitivity
2.1 Warm‐Sensitive Neurons
2.2 Cold‐Sensitive Neurons
2.3 Temperature‐Insensitive Neurons
3 Neuronal Integration of Central and Peripheral Temperature
Figure 1. Figure 1.

Effects of endogenous factors on three different types of neurons recorded in rat preoptic tissue slices. Each record shows the neuron's firing rate (impulses/second) and tissue temperature (°C). A: temperature‐insensitive neuron. B: warm‐sensitive neuron. C: cold‐sensitive neuron. Bars above records indicate times when tissue perfusion was switched from normal medium to experimental medium containing: T, testosterone; E, estradiol; C, ethanol control; O, hyperosmotic (309 mOsm); or G, low glucose (1 mM).

From Boulant and Silva 23
Figure 2. Figure 2.

Preoptic warm‐sensitive neuron recorded in a rat hypothalamic tissue slice before (1), during (2), and after (3) synaptic blockade with high‐magnesium‐low‐calcium perfusion. Top: record of firing rate and slice temperature. Connected arrows indicate switches from perfusions with normal medium to synaptic blockade medium. Bottom: thermoresponses curves for the three conditions shown in the record.

From Kelso and Boulant 71
Figure 3. Figure 3.

Firing rate of a delayed cold‐sensitive neuron recorded in vitro from the posterior hypothalamus. Record shows integrated firing rate and tissue temperature. Connected arrows indicate switches from perfusion with normal medium to two experimental media: synaptic blockade with high‐magnesium‐low‐calcium medium or blockade of the Na+/K+‐pump by 10−6M ouabain.

From Dean and Boulant 35
Figure 4. Figure 4.

Intracellular activity of a preoptic warm‐sensitive neuron recorded at three different temperatures. Resting membrane potential is approximately −60 mV and does not change with temperature. A: amplified record showing depolarizing pacemaker potentials generating action potentials (which are truncated). Arrows indicate IPSPs. B: similar activity in the same neuron, except all interspike intervals are prolonged and contain IPSPs. C: averaged prespike and postspike activity, showing that cooling decreases the pacemaker potential's rate of rise. Each temperature shows the average of 15 action potentials superimposed on threshold. D: averaged IPSP activity, showing that cooling increases the amplitude and duration of the postsynaptic potential. Each temperature shows the average of 16–19 IPSPs.

From Curras, Kelso, and Boulant 32
Figure 5. Figure 5.

Effect of temperature on intracellularly recorded cold‐sensitive neuronal activity. A: action potentials and postsynaptic potentials in a preoptic cold‐sensitive neuron. Action potentials are truncated to show amplified postsynaptic potentials. Note the general lack of depolarizing prepotentials that are observed in warm‐sensitive neurons. Bottom graphs show the effect of temperature on the frequencies (events/second) of EPSPs (circles) and IPSPs (triangles). B: the same neuron shown in A appears to be excited by another cold‐sensitive neuron. C: a different preoptic cold‐sensitive neuron, which appears to be inhibited by a warm‐sensitive neuron.

From Curras, Kelso, and Boulant 32
Figure 6. Figure 6.

Effect of temperature on a preoptic temperature‐insensitive neuron. A: firing rate as a function of tissue temperature. B: averaged prespike and postspike activity at two different temperatures. Each temperature shows the average of 15 action potentials superimposed on the spike threshold. Warming decreased spike amplitude (height shown by arrow) and afterhyperpolarizing potential. C and D show the same neuron's activity during constant injection of depolarizing current. C: depolarization increased both firing rate and thermosensitivity. D: depolarization also altered effect of temperature on pacemaker potential's rate of rise.

From Curras, Kelso and Boulant 32
Figure 7. Figure 7.

Ouabain blockade of the Na+/K+‐pump produces increased firing rate and thermosensitivity in a temperature‐insensitive neuron recorded in vitro in the lateral preoptic area. Top records show firing rate and tissue temperature. Connected arrows indicate switches from perfusion with normal medium to 10−6 M ouabain. Bottom graphs show changes in firing rate and thermosensitivity during the six periods indicated in the top record.

From Curras and Boulant 31
Figure 8. Figure 8.

Preoptic neuronal responses (A and C) and whole‐body thermoregulatory responses (B and D) to changes in preoptic temperature (Tpo) and extrahypothalamic (skin or spinal) temperature. Each graph shows the effect of skin or spinal temperature on the hypothalamic thermosensitivity of neuronal and whole‐body responses. A: Firing rate (FR) of a warm‐sensitive neuron (W) as a function of Tpo. B: Heat loss response as a function of Tpo, C: Firing rate of a cold‐sensitive neuron (C) as a function of Tpo. D: Heat production as a function of Tpo. All responses to Tpo are shown at warm (w), cold (c), and neutral (n) skin or spinal temperatures. (+), excitatory input; (−), inhibitory input.

From Boulant and Gonzalez 18
Figure 9. Figure 9.

Relationship between neuronal firing rate and range of thermosensitivity. A: average thermo‐response curves of 86 warm‐sensitive neurons recorded in rabbit PO/AH. Neurons were placed into five groups based on their spontaneous firing rates at 38°C (FR38°), that is, the average core temperature in an anesthetized rabbit. Values above each section indicate the slopes over each temperature range. B: neuronal model showing hypothesized thermoregulatory roles for warm‐sensitive neurons (W) and cold‐sensitive neurons (C), based on each neuron's range ofthermosensitivity. (+), excitatory input; (−), inhibitory input. F, firing rate; T, preoptic temperature; dashed line, thermoneutral preoptic temperature.

From Boulant 10. Modified from Boulant 8
Figure 10. Figure 10.

Modification to part of the neuronal model in Figure 9, showing two different groups of PO/AH neurons controlling different heat production responses. This model proposes that neurons controlling shivering are influenced less by afferent thermal input and more by nonsynaptic endogenous factors. Neurons controlling shivering also have lower threshold temperatures and synaptically excite cold‐sensitive spinal neurons. Note that some species show opposite responses such that shivering and nonshivering responses could be interchanged, depending on the species.

From Boulant, Curras and Dean 15


Figure 1.

Effects of endogenous factors on three different types of neurons recorded in rat preoptic tissue slices. Each record shows the neuron's firing rate (impulses/second) and tissue temperature (°C). A: temperature‐insensitive neuron. B: warm‐sensitive neuron. C: cold‐sensitive neuron. Bars above records indicate times when tissue perfusion was switched from normal medium to experimental medium containing: T, testosterone; E, estradiol; C, ethanol control; O, hyperosmotic (309 mOsm); or G, low glucose (1 mM).

From Boulant and Silva 23


Figure 2.

Preoptic warm‐sensitive neuron recorded in a rat hypothalamic tissue slice before (1), during (2), and after (3) synaptic blockade with high‐magnesium‐low‐calcium perfusion. Top: record of firing rate and slice temperature. Connected arrows indicate switches from perfusions with normal medium to synaptic blockade medium. Bottom: thermoresponses curves for the three conditions shown in the record.

From Kelso and Boulant 71


Figure 3.

Firing rate of a delayed cold‐sensitive neuron recorded in vitro from the posterior hypothalamus. Record shows integrated firing rate and tissue temperature. Connected arrows indicate switches from perfusion with normal medium to two experimental media: synaptic blockade with high‐magnesium‐low‐calcium medium or blockade of the Na+/K+‐pump by 10−6M ouabain.

From Dean and Boulant 35


Figure 4.

Intracellular activity of a preoptic warm‐sensitive neuron recorded at three different temperatures. Resting membrane potential is approximately −60 mV and does not change with temperature. A: amplified record showing depolarizing pacemaker potentials generating action potentials (which are truncated). Arrows indicate IPSPs. B: similar activity in the same neuron, except all interspike intervals are prolonged and contain IPSPs. C: averaged prespike and postspike activity, showing that cooling decreases the pacemaker potential's rate of rise. Each temperature shows the average of 15 action potentials superimposed on threshold. D: averaged IPSP activity, showing that cooling increases the amplitude and duration of the postsynaptic potential. Each temperature shows the average of 16–19 IPSPs.

From Curras, Kelso, and Boulant 32


Figure 5.

Effect of temperature on intracellularly recorded cold‐sensitive neuronal activity. A: action potentials and postsynaptic potentials in a preoptic cold‐sensitive neuron. Action potentials are truncated to show amplified postsynaptic potentials. Note the general lack of depolarizing prepotentials that are observed in warm‐sensitive neurons. Bottom graphs show the effect of temperature on the frequencies (events/second) of EPSPs (circles) and IPSPs (triangles). B: the same neuron shown in A appears to be excited by another cold‐sensitive neuron. C: a different preoptic cold‐sensitive neuron, which appears to be inhibited by a warm‐sensitive neuron.

From Curras, Kelso, and Boulant 32


Figure 6.

Effect of temperature on a preoptic temperature‐insensitive neuron. A: firing rate as a function of tissue temperature. B: averaged prespike and postspike activity at two different temperatures. Each temperature shows the average of 15 action potentials superimposed on the spike threshold. Warming decreased spike amplitude (height shown by arrow) and afterhyperpolarizing potential. C and D show the same neuron's activity during constant injection of depolarizing current. C: depolarization increased both firing rate and thermosensitivity. D: depolarization also altered effect of temperature on pacemaker potential's rate of rise.

From Curras, Kelso and Boulant 32


Figure 7.

Ouabain blockade of the Na+/K+‐pump produces increased firing rate and thermosensitivity in a temperature‐insensitive neuron recorded in vitro in the lateral preoptic area. Top records show firing rate and tissue temperature. Connected arrows indicate switches from perfusion with normal medium to 10−6 M ouabain. Bottom graphs show changes in firing rate and thermosensitivity during the six periods indicated in the top record.

From Curras and Boulant 31


Figure 8.

Preoptic neuronal responses (A and C) and whole‐body thermoregulatory responses (B and D) to changes in preoptic temperature (Tpo) and extrahypothalamic (skin or spinal) temperature. Each graph shows the effect of skin or spinal temperature on the hypothalamic thermosensitivity of neuronal and whole‐body responses. A: Firing rate (FR) of a warm‐sensitive neuron (W) as a function of Tpo. B: Heat loss response as a function of Tpo, C: Firing rate of a cold‐sensitive neuron (C) as a function of Tpo. D: Heat production as a function of Tpo. All responses to Tpo are shown at warm (w), cold (c), and neutral (n) skin or spinal temperatures. (+), excitatory input; (−), inhibitory input.

From Boulant and Gonzalez 18


Figure 9.

Relationship between neuronal firing rate and range of thermosensitivity. A: average thermo‐response curves of 86 warm‐sensitive neurons recorded in rabbit PO/AH. Neurons were placed into five groups based on their spontaneous firing rates at 38°C (FR38°), that is, the average core temperature in an anesthetized rabbit. Values above each section indicate the slopes over each temperature range. B: neuronal model showing hypothesized thermoregulatory roles for warm‐sensitive neurons (W) and cold‐sensitive neurons (C), based on each neuron's range ofthermosensitivity. (+), excitatory input; (−), inhibitory input. F, firing rate; T, preoptic temperature; dashed line, thermoneutral preoptic temperature.

From Boulant 10. Modified from Boulant 8


Figure 10.

Modification to part of the neuronal model in Figure 9, showing two different groups of PO/AH neurons controlling different heat production responses. This model proposes that neurons controlling shivering are influenced less by afferent thermal input and more by nonsynaptic endogenous factors. Neurons controlling shivering also have lower threshold temperatures and synaptically excite cold‐sensitive spinal neurons. Note that some species show opposite responses such that shivering and nonshivering responses could be interchanged, depending on the species.

From Boulant, Curras and Dean 15
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Article Title: Hypothalamic Neurons Regulating Body Temperature
 

How to Cite

Jack A. Boulant. Hypothalamic Neurons Regulating Body Temperature. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 105-126. First published in print 1996. doi: 10.1002/cphy.cp040106