Change In Thermal Preference Research Articles

Role of thermosensitive transient receptor potential (TRP) channels in thermal preference of male and female mice

Transient Receptor Potential (TRP) ion channels are important for sensing environmental temperature. In rodents, TRPV4 senses warmth (25-34 °C), TRPV1 senses heat (>42 °C), TRPA1 putatively senses cold (<17 °C), and TRPM8 senses cool-cold (18-26 °C). We investigated if knockout (KO) mice lacking these TRP channels exhibited changes in thermal preference. Thermal preference was tested using a dual hot-cold plate with one thermoelectric surface set at 30 °C and the adjacent surface at a temperature of 15–45 °C in 5 °C increments. Blinded observers counted the number of times mice crossed through an opening between plates and the percentage of time spent on the 30 °C plate. In a separate experiment, observers blinded as to genotype also assessed the temperature at the location on a thermal gradient (1.83 m, 4-50 °C) occupied by the mouse at 5- or 10-min intervals over 2 h. Male and female wildtype mice preferred 30 °C and significantly avoided colder (15–20 °C) and hotter (40–45 °C) temperatures. Male TRPV1KOs and TRPA1KOs, and TRPV4KOs of both sexes, were similar, while female WTs, TRPV1KOs, TRPA1KOs and TRPM8KOs did not show significant thermal preferences across the temperature range. Male and female TRPM8KOs did not significantly avoid the coldest temperatures. Male mice (except for TRPM8KOs) exhibited significantly fewer plate crossings at hot and cold temperatures and more crossings at thermoneutral temperatures, while females exhibited a similar but non-significant trend. Occupancy temperatures along the thermal gradient exhibited a broad distribution that shrank somewhat over time. Mean occupancy temperatures (recorded at 90–120 min) were significantly higher for females (30–34 °C) compared to males (26–27 °C) of all genotypes, except for TRPA1KOs which exhibited no sex difference. The results indicate (1) sex differences with females (except TRPA1KOs) preferring warmer temperatures, (2) reduced thermosensitivity in female TRPV1KOs, and (3) reduced sensitivity to cold and innocuous warmth in male and female TRPM8KOs consistent with previous studies.

Selection of preferred thermal environment and cold-avoidance responses in rats rely on signals transduced by the dorsal portion of the lateral funiculus of the spinal cord

ABSTRACT Thermoregulatory behaviors are powerful effectors for core body temperature (Tc) regulation. We evaluated the involvement of afferent fibers ascending through the dorsal portion of the lateral funiculus (DLF) of the spinal cord in “spontaneous” thermal preference and thermoregulatory behaviors induced by thermal and pharmacological stimuli in a thermogradient apparatus. In adult Wistar rats, the DLF was surgically severed at the first cervical vertebra bilaterally. The functional effectiveness of funiculotomy was verified by the increased latency of tail-flick responses to noxious cold (−18°C) and heat (50°C). In the thermogradient apparatus, funiculotomized rats showed a higher variability of their preferred ambient temperature(Tpr) and, consequently, increased Tc fluctuations, as compared to sham-operated rats. The cold-avoidance (warmth-seeking) response to moderate cold (whole-body exposure to ~17°C) or epidermal menthol (an agonist of the cold-sensitive TRPM8 channel) was attenuated in funiculotomized rats, as compared to sham-operated rats, and so was the Tc (hyperthermic) response to menthol. In contrast, the warmth-avoidance (cold-seeking) and Tc responses of funiculotomized rats to mild heat (exposure to ~28°C) or intravenous RN-1747 (an agonist of the warmth-sensitive TRPV4; 100 μg/kg) were unaffected. We conclude that DLF-mediated signals contribute to driving spontaneous thermal preference, and that attenuation of these signals is associated with decreased precision of Tc regulation. We further conclude that thermally and pharmacologically induced changes in thermal preference rely on neural, presumably afferent, signals that travel in the spinal cord within the DLF. Signals conveyed by the DLF are important for cold-avoidance behaviors but make little contribution to heat-avoidance responses.

Differential modulation of thermal preference after sensitization by optogenetic or pharmacological activation of heat-sensitive nociceptors.

Common approaches to studying mechanisms of chronic pain and sensory changes in pre-clinical animal models involve measurement of acute, reflexive withdrawal responses evoked by noxious stimuli. These methods typically do not capture more subtle changes in sensory processing nor report on the consequent behavioral changes. In addition, data collection and analysis protocols are often labour-intensive and require direct investigator interactions, potentially introducing bias. In this study, we develop and characterize a low-cost, easily assembled behavioral assay that yields self-reported temperature preference from mice that is responsive to peripheral sensitization. This system uses a partially automated and freely available analysis pipeline to streamline the data collection process and enable objective analysis. We found that after intraplantar administration of the TrpV1 agonist, capsaicin, mice preferred to stay in cooler temperatures than saline injected mice. We further observed that gabapentin, a non-opioid analgesic commonly prescribed to treat chronic pain, reversed this aversion to higher temperatures. In contrast, optogenetic activation of the central terminals of TrpV1+ primary afferents via in vivo spinal light delivery did not induce a similar change in thermal preference, indicating a possible role for peripheral nociceptor activity in the modulation of temperature preference. We conclude that this easily produced and robust sensory assay provides an alternative approach to investigate the contribution of central and peripheral mechanisms of sensory processing that does not rely on reflexive responses evoked by noxious stimuli.

Dehydration constrains thermoregulation and space use in lizards.

Climate change is negatively affecting many species. The increase in mean air temperature is often associated with shifts in distribution, changes in phenology, and local extinctions. Other factors that only partially correlate with air temperature, like water shortage, may also contribute to the negative consequences of climate change. Although the effect of temperature on lizards’ ecophysiology is highly studied, many lizards are also at risks of increased water loss and dehydration, which are predicted to increase under climate change. Here we aimed for the first time to explore if lacertid lizards exposed to dehydration thermoregulate less precisely than hydrated lizards and if dehydrated lizards are less active, change the daily pattern of thermoregulation and balance water balance against thermoregulation. We exposed four lizard species with differences in the thermal preference to thermal gradients with or without a source of water. We measured preferred body temperatures, daily pattern of thermoregulation, and the use of space. Dehydration negatively affected thermoregulation in all investigated species. Dehydrated lizards reduced their preferred body temperature and showed a species-specific pattern of hourly change in thermal preference. Furthermore, they more frequently used the colder parts of the gradients and spent more time hidden. Lizards experiencing dehydration may suffer a reduction in survival and fitness because of poor thermoregulation. Similarly, they may spend more time hidden, waiting for more favourable weather conditions. Such inactivity may carry ecological costs especially in those regions that undergo either short or prolonged periods of droughts.

A Switch in Thermal Preference in Drosophila Larvae Depends on Multiple Rhodopsins

Drosophila third-instar larvae exhibit changes in their behavioral responses to gravity and food as they transition from feeding to wandering stages. Using a thermal gradient encompassing the comfortable range (18°C to 28°C), we found that third-instar larvae exhibit a dramatic shift in thermal preference. Early third-instar larvae prefer 24°C, which switches to increasingly stronger biases for 18°C-19°C in mid- and late-third-instar larvae. Mutations eliminating either of two rhodopsins, Rh5 and Rh6, wiped out these age-dependent changes in thermal preference. In larvae, Rh5 and Rh6 are thought to function exclusively in the light-sensing Bolwig organ. However, the Bolwig organ was dispensable for the thermal preference. Rather, Rh5 and Rh6 were required intrpA1-expressing neurons in the brain, ventral nervecord, and body wall. Because Rh1 contributes tothermal selection in the comfortable range during the early to mid-third-instar stage, fine thermal discrimination depends on multiple rhodopsins.

Diurnal and Seasonal Changes in Thermal Preference of Single, Isolated Bees and Small Groups of Bees (Apis mellifera L.)

The aim of the present study was: to compare thermoregulatory behaviour of single honeybee workers and groups of 3–15 bees over their annual activity period and to check out whether the annual fluctuations of ambient temperature selection are correlated with phases of the colony development. Thermal behaviour of both single workers and groups of bees was recorded, using a video camera, in a thermal gradient system. Thermal preferences of the insects were tested seasonally in spring (May/June), summer (July/August) and autumn (September–November). Both single bees and small groups of bees changed their thermal behaviour in daily cycle. The season of the year had distinct effect on temperature preferences of both single honeybee workers or small groups of bees. In single honeybee workers the lowest ambient temperatures were preferred in late spring (the swarming phase) while the highest temperatures were selected during the summer (the colony growing phase). There were significant seasonal changes in ambient temperature selected by groups of honeybee workers. Groups of honeybee workers tended to prefer the lowest temperatures in late spring and the highest temperatures were selected during the summer. The day-night differences exhibited by small groups of bees in our experiments are likely to represent behavioural responses of the honeybee colony. In our experiments we proved an influence of the season of the year on the honeybees’ thermal behaviour, which might be connected with seasonal shifts of temperature regulated by the honeybee colony.

Behavioural fever is a synergic signal amplifying the innate immune response

Behavioural fever, defined as an acute change in thermal preference driven by pathogen recognition, has been reported in a variety of invertebrates and ectothermic vertebrates. It has been suggested, but so far not confirmed, that such changes in thermal regime favour the immune response and thus promote survival. Here, we show that zebrafish display behavioural fever that acts to promote extensive and highly specific temperature-dependent changes in the brain transcriptome. The observed coupling of the immune response to fever acts at the gene–environment level to promote a robust, highly specific time-dependent anti-viral response that, under viral infection, increases survival. Fish that are not offered a choice of temperatures and that therefore cannot express behavioural fever show decreased survival under viral challenge. This phenomenon provides an underlying explanation for the varied functional responses observed during systemic fever. Given the effects of behavioural fever on survival and the fact that it exists across considerable phylogenetic space, such immunity–environment interactions are likely to be under strong positive selection.

Working with what you’ve got: Changes in thermal preference and behavior in mice with or without nesting material

In laboratories mice are typically housed at ambient temperatures ( T a) of 20–24 °C, which are below their average preferred T a of ≈30 °C. Adjusting laboratory T a is not a solution because preferences differ depending on activity, time of the day, and gender. We tested the hypothesis that providing mice with nesting material will allow behavioral thermoregulation and reduce aversion to colder T a. We housed C57BL/6J mice with and without nesting material in a set of 3 connected cages, each maintained at a different T a (20, 25, or 30 °C). Mice were confined in and given free access to the T a options to determine if thermotaxis or nest building was the primary mode of behavioral thermoregulation. As predicted, nesting material reduced aversion to 20 °C but the overall preference, in both treatments, was still 30 °C. Inactive and nesting behaviors were more likely to be seen in contact with nesting material while active behaviors were more likely to be observed when not in contact. Nest quality increased with decreasing T a when mice could not use thermotaxis but nest quality was uncorrelated with T a when thermotaxis was possible. Males decreased nest quality with increasing temperatures but females showed no correlation. We conclude that nesting material does not alter thermal preferences for 30 °C when thermotaxis is possible, indicating thermotaxis as the primary mode of behavioral thermoregulation. However, when thermotaxis is not possible, mice adjust nest shape depending on the T a. Nesting material appears to partially compensate for cooler T a and is especially important when mice are inactive. Therefore, nesting material may be a solution to the mismatch between laboratory T a and mouse thermal preferences.

Size-dependent thermal preferences in a pelagic fish

Large fish often inhabit colder waters than small fish. Using a simple bioenergetic model, we found that the optimal temperature for growth should decrease with increasing body size. We predicted that this mechanism would produce an ontogenetic change in thermal preference and then tested our predictions with Pacific salmon, Oncorhynchus spp. In a laboratory experiment, the slope of a regression of growth increment on initial size became steeper with increasing temperature, so that the optimal temperature for growth decreased with increasing body size. In field observations, larger and older salmon inhabited cooler areas, whereas smaller and younger salmon inhabited warmer areas. These patterns were consistent with a size-dependent effect of temperature on condition factor, a parameter shown experimentally to be a measure of the most recent growth performance. Temperatures for maximising condition factor were lower for larger fish. Thus, an ontogenetic change in individual thermal preference toward cooler areas maximises the growth performance of fish, and the negative effects of climate warming on growth are hypothesised to be more severe for larger fish.

The changes in thermal preference, sleep–wakefulness, body temperature and locomotor activity in the rats with medial septal lesion

The effects of the destruction of the medial septal neurons (MS) with N-methyl- d-aspartic acid on sleep–wakefulness (S–W), body temperature ( T b), locomotor activity (LMA) and thermal preference were studied in male Wistar rats. When these rats were given a choice of three ambient temperatures ( T amb) of 24, 27 and 30 °C, they preferred 27 °C before the lesion. But they chose 30 °C during the initial days and 24 °C by the third week after the MS lesion. The MS lesion produced an increase in paradoxical sleep (PS) though this change was not very evident when the rats were not allowed to choose their T amb. Though there was a decrease in slow wave sleep (SWS), it recovered considerably, when the lesioned rats chose their preferred T amb. However, the frequency of SWS episodes did not show any recovery. There was a decrease in both T b and LMA by the third week after the MS lesion. It can, therefore, be concluded that the MS lesion affected the initiation of SWS, as there was a decrease in the frequency of SWS episodes. Study of S–W in the rats that were given freedom to select T amb helped to demonstrate the role of the MS in the inhibition of PS. It also showed that the thermostat of the rats was reset at a lower level by the third week after the MS lesion. Decrease in heat production resulting from a decrease in LMA, could have contributed towards the animals’ efforts to maintain a lower T b.

Enhanced thermal avoidance in mice lacking the ATP receptor P2X 3

P2X 3 is an ATP-gated cation channel subtype expressed by a subpopulation of primary sensory neurons. In vivo spinal cord recordings in mice lacking P2X 3 ( P 2 X 3 − / − ) have suggested that this protein may be important for the coding of peripheral warm stimuli. To explore this possibility more thoroughly, we examined behavioral and electrophysiological responses to thermal stimuli in P 2 X 3 − / − mice. As previously reported, recording from the spinal cord dorsal horn of anesthetized P 2 X 3 − / − mice revealed a blunted response of wide dynamic range neurons to hind paw heating. When placed in a thermal gradient, however, P 2 X 3 − / − mice exhibited an unexpectedly enhanced avoidance of both hot and cold temperatures, relative to controls. In the tail immersion test, mutant mice exhibited shorter withdrawal latencies at temperatures above and below thermoneutrality. Consistent with these changes, P 2 X 3 − / − mice exhibited enhanced induction of spinal cord c-FOS following hind paw heating to 45 °C. Thus, gain- and loss-of-function thermosensory phenotypes coexist in P 2 X 3 − / − mice. No changes in thermal preference were observed in wild-type mice injected subcutaneously with the P2X 3 antagonist, A317491 or intrathecally with the P2X 3 and P2X 1 antagonist TNP-ATP. The reason for this apparent discrepancy is unclear, but we cannot exclude the possibility that compensatory events contribute, at least in part, to the P 2 X 3 − / − phenotype. Regardless, this study illustrates the utility of thermal preference assays as part of a comprehensive approach to the analysis of mouse thermosensation.

Changes in thermal preference, sleep–wakefulness, body temperature and locomotor activity of rats during continuous recording for 24 hours

This study was aimed at correlating diurnal changes in thermal preference of rats with their body temperature ( T b), sleep–wakefulness (S–W) and locomotor activity (LMA). Electroencephalogram (EEG), electromyogram (EMG), electrooculogram (EOG) and T b were recorded by telemetry, while an activity monitor measured LMA and thermal preference. A special environmental chamber, which was designed and fabricated, enabled for the first time, simultaneous measurement of thermal preference, along with S–W and T b. S–W, thermal preference and LMA were recorded continuously in six adult male Wistar rats, for 24 h, for 3 days, and T b with thermal preference and LMA were recorded for another 3 days. LMA and T b were higher at night than during day. The rats slept less during the night time. Increased frequency of sleep episodes contributed towards increased sleep during day time. They preferred an ambient temperature ( T amb) of 24 °C at night and 27 °C during the day. Though the preference for higher T amb during day time coincided with increased sleep, the rats did not move over to higher T amb prior to the onset of sleep episodes. Though the diurnal alterations in sleep, T b and LMA were similar to those reports from animals kept in constant T amb, the day–night variation of paradoxical sleep (PS) was exaggerated when the rats selected their own preferred T amb.

Temperature Preference and Responses of Cutaneous Temperature-Sensitive Neurons during Bullfrog Development

The mean temperature selected by bullfrog tadpoles, Rana catesbeiana, in a continuous thermal gradient increased as a function of development; from 24 C at TaylorKollros stages X-XII, to 29 C at stages XIX-XX, to 32 C at stages XXIV-XXV. The variance of the selected body temperature decreased and the frequency at the modal temperature increased as development proceeded. Responses of a total of 29 cold-and three warm-sensitive neurons were characterized. As development progressed, the temperature at which static impulse frequency occurred in individual cutaneous coldsensitive neurons increased from a low of 16 C at stage XIII to as high as 32 C at stage XXV. The average static maximum temperature of these cold-sensitive units was less than the mean selected body temperature at each developmental stage studied (17 C at XIII-XIV, 25 C at XIX-XX, and 27 C at XXIV-XXV) but paralleled the developmental changes in thermal preference. We hypothesize that the ontogeny of the final thermal preferendum of bullfrogs is dependent on the developmental changes in the thermal characteristics of peripheral cold-sensitive neurons as well as possible changes in peripheral warm-sensitive neurons and neurons within the central nervous system.

Set-point displacement for behavioural thermoregulation in anorexia nervosa.

1. The temperatures of thermal stimuli which evoked a feeling of maximal pleasantness upon contact with the hands of 14 malnourished patients with anorexia nervosa and 19 control subjects have been determined. A uniform skin temperature of 35 degrees C for all individuals studied was achieved by immersion of the subjects and patients in water at that temperature. Core temperatures of the anorexia patients were similar to those of the control subjects, but six of the patients preferred temperatures that were significantly higher than those of the control subjects. The thermal preferences of the remainder of the patients were similar to those of the control subjects. 2. The abnormally high thermal preferences of some of the anorexic patients could not be attributed to abnormal thyroid status, since values for serum free thyroxine measured in this group were similar to those obtained for the remaining patients. The abnormal responses persisted after there had been a substantial gain in the patients' weight and did not therefore appear to be directly due to malnutrition. 3. Elevation of deep body temperature produced an expected shift in preference towards lower stimulus temperatures in a sample of subjects from the control group, and in the patients who had initially preferred temperatures within the range of the controls. In the patients who had initially preferred abnormally high stimulus temperatures, however, hyperthermia produced little change in thermal preference. 4. It is suggested that an elevation in the set-point temperature for behavioural thermoregulation can occur in some patients with anorexia nervosa, and that this displacement may contribute to the distressing sense of cold which some patient experience.

Thermal preferences of hatchling new Guinea crocodiles: Effects of feeding and ontogeny

1. 1. The body temperatures ( T bs) and thermal behavior of hatchling New Guinea crocodiles ( Crocodylus novaeguineae) were monitored in a terrestrial-aquatic thermal gradient exposed to the natural photoperiod. 2. 2. At 0–2 weeks of age, hatchlings selected T bs of 33.4–33.9°C that were significantly elevated by 1.4–2.9°C above levels preferred subsequently. Higher T bs were pronounced during the period of yolk absorption and may have facilitated the rapid assimilation of unabsorbed yolk immediately after hatching. A similar thermophilic response has been noted for hatchlings of two other species of crocodilians. 3. 3. At 2–5 weeks of age, hatchlings selected lower T bs (31.8–32.2°C) relative to previous values. T bs were not elevated or less variable in response to feeding and an increase in heat-seeking behavior was not apparent. 4. 4. Hatchings (2–5-weeks old) preferred T bs that were approx 2°C higher than the T bs maintained by a juvenile and adults monitored in a natural setting. Thermal preference in New Guinea crocodiles appeared to decline to adult levels within the first two years of life. 5. 5. Ontogenetic changes in thermal preference, particularly thermophily during early life, are evident in this crocodilian species and may occur in other reptiles as well.