An official website of the United States government
Abstract Neurons that participate in sensory processing often display “ON” responses, i.e., fire transiently at the onset of a stimulus. ON transients are widespread, perhaps universal to sensory coding, yet their function is not always well-understood. Here, we show that ON responses in theDrosophilathermosensory system extrapolate the trajectory of temperature change, priming escape behavior if unsafe thermal conditions are imminent. First, we show that second-order thermosensory projection neurons (TPN-IIIs) and their Lateral Horn targets (TLHONs), display ON responses to thermal stimuli, independent of direction of change (heating or cooling) and of absolute temperature. Instead, they track the rate of temperature change, with TLHONs firing exclusively to rapid changes (>0.2 °C/s). Next, we use connectomics to track TLHONs’ output to descending neurons that control walking and escape, and modeling and genetic silencing to demonstrate how ON transients can flexibly amplify aversive responses to small thermal change. Our results suggest that, across sensory systems, ON transients may represent a general mechanism to systematically anticipate and respond to salient or dangerous conditions.
more »
« less
Temperature sensitivity and temperature response across development in the Drosophila larva
The surrounding thermal environment is highly important for the survival and fitness of animals, and as a result most exhibit behavioral and neural responses to temperature changes. We study signals generated by thermosensory neurons inDrosophilalarvae and also the physical and sensory effects of temperature variation on locomotion and navigation. In particular we characterize how sensory neuronal and behavioral responses to temperature variation both change across the development of the larva. Looking at a wide range of non-nociceptive isotropic thermal environments, we characterize the dependence of speed, turning rate, and other behavioral components on temperature, distinguishing the physical effects of temperature from behavior changes based on sensory processing. We also characterize the strategies larvae use to modulate individual behavioral components to produce directed navigation along thermal gradients, and how these strategies change during physical development. Simulations based on modified random walks show where thermotaxis in each developmental stage fits into the larger context of possible navigation strategies. We also investigate cool sensing neurons in the larva's dorsal organ ganglion, characterizing neural response to sine-wave modulation of temperature while performing single-cell-resolution 3D imaging. We determine the sensitivity of these neurons, which produce signals in response to extremely small temperature changes. Combining thermotaxis results with neurophysiology data, we observe, across development, sensitivity to temperature change as low as a few thousandths of a °C per second, or a few hundredths of a °C in absolute temperature change.
more »
« less
- Award ID(s):
- 2144385
- PAR ID:
- 10515798
- Date Published:
- Journal Name:
- Frontiers in Molecular Neuroscience
- Volume:
- 16
- ISSN:
- 1662-5099
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Ahamed, Tosif (Ed.)Motile organisms actively detect environmental signals and migrate to a preferable environment. Especially, small animals convert subtle spatial difference in sensory input into orientation behavioral output for directly steering toward a destination, but the neural mechanisms underlying steering behavior remain elusive. Here, we analyze a C . elegans thermotactic behavior in which a small number of neurons are shown to mediate steering toward a destination temperature. We construct a neuroanatomical model and use an evolutionary algorithm to find configurations of the model that reproduce empirical thermotactic behavior. We find that, in all the evolved models, steering curvature are modulated by temporally persistent thermal signals sensed beyond the time scale of sinusoidal locomotion of C . elegans . Persistent rise in temperature decreases steering curvature resulting in straight movement of model worms, whereas fall in temperature increases curvature resulting in crooked movement. This relation between temperature change and steering curvature reproduces the empirical thermotactic migration up thermal gradients and steering bias toward higher temperature. Further, spectrum decomposition of neural activities in model worms show that thermal signals are transmitted from a sensory neuron to motor neurons on the longer time scale than sinusoidal locomotion of C . elegans . Our results suggest that employments of temporally persistent sensory signals enable small animals to steer toward a destination in natural environment with variable, noisy, and subtle cues.more » « less
-
Detailed descriptions of behavior provide critical insight into the structure and function of nervous systems. InDrosophilalarvae and many other systems, short behavioral experiments have been successful in characterizing rapid responses to a range of stimuli at the population level. However, the lack of long-term continuous observation makes it difficult to dissect comprehensive behavioral dynamics of individual animals and how behavior (and therefore the nervous system) develops over time. To allow for long-term continuous observations in individual fly larvae, we have engineered a robotic instrument that automatically tracks and transports larvae throughout an arena. The flexibility and reliability of its design enables controlled stimulus delivery and continuous measurement over developmental time scales, yielding an unprecedented level of detailed locomotion data. We utilize the new system’s capabilities to perform continuous observation of exploratory search behavior over a duration of 6 hr with and without a thermal gradient present, and in a single larva for over 30 hr. Long-term free-roaming behavior and analogous short-term experiments show similar dynamics that take place at the beginning of each experiment. Finally, characterization of larval thermotaxis in individuals reveals a bimodal distribution in navigation efficiency, identifying distinct phenotypes that are obfuscated when only analyzing population averages.more » « less
-
null (Ed.)The environment experienced during embryonic development is a rich source of phenotypic variation, as environmental signals have the potential to both inform adaptive plastic responses and disrupt normal developmental programs. Environment-by-embryo interactions are particularly consequential for species with temperature-dependent sex determination, a mode of sex determination common in non-avian reptiles and fish, in which thermal cues during a discrete period of development drive the formation of either an ovary or a testis. Here we examine the impact of thermal variation during incubation in combination with developmental exposure to a common endocrine-disrupting contaminant on fitness-related hatchling traits in the American alligator (Alligator mississippiensis), a species with temperature-dependent sex determination. Using a factorial design, we exposed field-collected eggs to five thermal profiles (three constant temperatures, two fluctuating temperatures) and two environmentally relevant doses of the pesticide metabolite dichlorodiphenyldichloroethylene; and we quantified incubation duration, sex ratios, hatchling morphometric traits, and growth (9–10 days post-hatch). Whereas dichlorodiphenyldichloroethylene exposure did not generally affect hatchling traits, constant and fluctuating temperatures produced diverse phenotypic effects. Thermal fluctuations led to subtle changes in incubation duration and produced shorter hatchlings with smaller heads when compared to the constant temperature control. Warmer, male-promoting incubation temperatures resulted in larger hatchlings with more residual yolk reserves when compared to cooler, female-promoting temperatures. Together, these findings advance our understanding of how complex environmental factors interact with developing organisms to generate phenotypic variation and raise questions regarding the mechanisms connecting variable thermal conditions to responses in hatchling traits and their evolutionary implications for temperature-dependent sex determination.more » « less
-
null (Ed.)Abstract Temperature is one of the most fundamental physical properties to characterize various physical, chemical, and biological processes. Even a slight change in temperature could have an impact on the status or dynamics of a system. Thus, there is a great need for high-precision and large-dynamic-range temperature measurements. Conventional temperature sensors encounter difficulties in high-precision thermal sensing on the submicron scale. Recently, optical whispering-gallery mode (WGM) sensors have shown promise for many sensing applications, such as thermal sensing, magnetic detection, and biosensing. However, despite their superior sensitivity, the conventional sensing method for WGM resonators relies on tracking the changes in a single mode, which limits the dynamic range constrained by the laser source that has to be fine-tuned in a timely manner to follow the selected mode during the measurement. Moreover, we cannot derive the actual temperature from the spectrum directly but rather derive a relative temperature change. Here, we demonstrate an optical WGM barcode technique involving simultaneous monitoring of the patterns of multiple modes that can provide a direct temperature readout from the spectrum. The measurement relies on the patterns of multiple modes in the WGM spectrum instead of the changes of a particular mode. It can provide us with more information than the single-mode spectrum, such as the precise measurement of actual temperatures. Leveraging the high sensitivity of WGMs and eliminating the need to monitor particular modes, this work lays the foundation for developing a high-performance temperature sensor with not only superior sensitivity but also a broad dynamic range.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.3389/fnmol.2023.1275469
