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1. Temperature sensitivity and temperature response across development in the Drosophila larva

   https://doi.org/10.3389/fnmol.2023.1275469  

   Evans, Anastasiia; Ferrer, Anggie J; Fradkov, Erica; Shomar, Joseph W; Forer, Josh; Klein, Mason (October 2023, Frontiers in Molecular Neuroscience)

   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. 

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2. The AMsh glia of C. elegans modulates the duration of touch-induced escape responses

   https://doi.org/10.1101/2023.12.13.571291  

   Awe, Temitope; Akinosho, Aalimah; Niha, Shifat; Kelly, Laura; Adams, Jessica; Stein, Wolfgang; Vidal-Gadea, Andrés (December 2023, bioRxiv)

   Abstract Once considered mere structural support cells in the nervous system, glia have recently been demonstrated to play pivotal roles in sensorimotor processing and to directly respond to sensory stimuli. However, their response properties and contributions to sensory-induced behaviors remain little understood. InCaenorhabditis elegans, the amphid sheath glia (AMsh) directly respond to aversive odorants and mechanical stimuli, but their precise transduction machinery and their behavioral relevance remain unclear. We investigated the role of AMsh in mechanosensation and their impact on escape behaviors inC. elegans. We found that nose touch stimuli in immobilized animals induced a slow calcium wave in AMsh, which coincided with the termination of escape reversal behaviors. Genetic ablation of AMsh resulted in prolonged reversal durations in response to nose touch, but not to harsh anterior touch, highlighting the specificity of AMsh’s role in distinct escape behaviors. Mechanotransduction in AMsh requires the α-tubulin MEC-12 and the ion channels ITR-1 and OSM-9, indicating a unique mechanosensory pathway that is distinct from the neighboring ASH neurons. We find that GABAergic signaling mediated by the GABA-A receptor orthologs LGC-37/8 and UNC-49 play a crucial role in modulating the duration of nose touch-induced reversals. We conclude that in addition to aversive odorant detection, AMsh mediate mechanosensation, play a pivotal role in terminating escape responses to nose touch, and provide a mechanism to maintain high sensitivity to polymodal sensory stimuli. SignificancePolymodal nociceptive sensory neurons have the challenge of multitasking across sensory modalities. They must respond to dangerous stimuli of one modality, but also adapt to repeated nonthreatening stimuli without compromising sensitivity to harmful stimuli from different modalities. Here we show that a pair of glia in the nematodeC. elegansmodulate the duration of nose-touch induced escape responses. We identify several molecules involved in the transduction of mechanical stimuli in these cells and show that they use the signaling molecule GABA to modulate neural function. We propose a mechanism through which these glia might function to maintain this polysensory neuron responsive to dangerous stimuli across different modalities. 

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3. Cortical coding of gustatory and thermal signals in active licking mice

   https://doi.org/10.1113/JP287499  

   Nash, Audrey_N; Shakeshaft, Morgan; Bouaichi, Cecilia_G; Odegaard, Katherine_E; Needham, Tom; Bauer, Martin; Bertram, Richard; Vincis, Roberto (January 2025, The Journal of Physiology)

   AbstractEating behaviours are influenced by the integration of gustatory, olfactory and somatosensory signals, which all contribute to the perception of flavour. Although extensive research has explored the neural correlates of taste in the gustatory cortex (GC), less is known about its role in encoding thermal information. This study investigates the encoding of oral thermal and chemosensory signals by GC neurons compared to the oral somatosensory cortex. In this study we recorded the spiking activity of more than 900 GC neurons and 500 neurons from the oral somatosensory cortex in mice allowed to freely lick small drops of gustatory stimuli or deionized water at varying non‐nociceptive temperatures. We then developed and used a Bayesian‐based analysis technique to assess neural classification scores based on spike rate and phase timing within the lick cycle. Our results indicate that GC neurons rely predominantly on rate information, although phase information is needed to achieve maximum accuracy, to effectively encode both chemosensory and thermosensory signals. GC neurons can effectively differentiate between thermal stimuli, excelling in distinguishing both large contrasts (14vs. 36°C) and, although less effectively, more subtle temperature differences. Finally a direct comparison of the decoding accuracy of thermosensory signals between the two cortices reveals that whereas the somatosensory cortex exhibited higher overall accuracy, the GC still encodes significant thermosensory information. These findings highlight the GC's dual role in processing taste and temperature, emphasizing the importance of considering temperature in future studies of taste processing.image Key pointsFlavour perception relies on gustatory, olfactory and somatosensory integration, with the gustatory cortex (GC) central to taste processing.GC neurons also respond to temperature, but the specifics of how the GC processes taste and oral thermal stimuli remain unclear.The focus of this study is on the role of GC neurons in the encoding of oral thermal information, particularly compared to the coding functions of the oral somatosensory cortex.We found that whereas the somatosensory cortex shows a higher classification accuracy for distinguishing water temperature, the GC still encodes a substantial amount of thermosensory information.These results emphasize the importance of including temperature as a key factor in future studies of cortical taste coding. 

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4. Convergent escape behaviour from distinct visual processing of impending collision in fish and grasshoppers

   https://doi.org/10.1113/JP284022  

   Dewell, Richard B; Carroll‐Mikhail, Terri; Eisenbrandt, Margaret R; Mendoza, Alexander F; Halder, Bidisha; Preuss, Thomas; Gabbiani, Fabrizio (October 2023, The Journal of Physiology)

   AbstractIn animal species ranging from invertebrate to mammals, visually guided escape behaviours have been studied using looming stimuli, the two‐dimensional expanding projection on a screen of an object approaching on a collision course at constant speed. The peak firing rate or membrane potential of neurons responding to looming stimuli often tracks a fixed threshold angular size of the approaching stimulus that contributes to the triggering of escape behaviours. To study whether this result holds more generally, we designed stimuli that simulate acceleration or deceleration over the course of object approach on a collision course. Under these conditions, we found that the angular threshold conveyed by collision detecting neurons in grasshoppers was sensitive to acceleration whereas the triggering of escape behaviours was less so. In contrast, neurons in goldfish identified through the characteristic features of the escape behaviours they trigger, showed little sensitivity to acceleration. This closely mirrored a broader lack of sensitivity to acceleration of the goldfish escape behaviour. Thus, although the sensory coding of simulated colliding stimuli with non‐zero acceleration probably differs in grasshoppers and goldfish, the triggering of escape behaviours converges towards similar characteristics. Approaching stimuli with non‐zero acceleration may help refine our understanding of neural computations underlying escape behaviours in a broad range of animal species.image Key pointsA companion manuscript showed that two mathematical models of collision‐detecting neurons in grasshoppers and goldfish make distinct predictions for the timing of their responses to simulated objects approaching on a collision course with non‐zero acceleration.Testing these experimental predictions showed that grasshopper neurons are sensitive to acceleration while goldfish neurons are not, in agreement with the distinct models proposed previously in these species using constant velocity approaches.Grasshopper and goldfish escape behaviours occurred after the stimulus reached a fixed angular size insensitive to acceleration, suggesting further downstream processing in grasshopper motor circuits to match what was observed in goldfish.Thus, in spite of different sensory processing in the two species, escape behaviours converge towards similar solutions.The use of object acceleration during approach on a collision course may help better understand the neural computations implemented for collision avoidance in a broad range of species. 

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5. Dynamic amplitude modulation of microstimulation evokes biomimetic onset and offset transients and reduces depression of evoked calcium responses in sensory cortices

   https://doi.org/10.1016/j.brs.2023.05.013  

   Hughes, Christopher; Kozai, Takashi (May 2023, Brain Stimulation)

   Background: Intracortical microstimulation (ICMS) is an emerging approach to restore sensation to people with neurological injury or disease. Biomimetic microstimulation, or stimulus trains that mimic neural activity in the brain through encoding of onset and offset transients, could improve the utility of ICMS for brain-computer interface (BCI) applications, but how biomimetic microstimulation affects neural activation is not understood. Current “biomimetic” ICMS trains aim to reproduce the strong onset and offset transients evoked in the brain by sensory input through dynamic modulation of stimulus parameters. Stimulus induced depression of neural activity (decreases in evoked intensity over time) is also a potential barrier to clinical implementation of sensory feedback, and dynamic microstimulation may reduce this effect. Objective: We evaluated how bio-inspired ICMS trains with dynamic modulation of amplitude and/or frequency change the calcium response, spatial distribution, and depression of neurons in the somatosensory and visual cortices. Methods: Calcium responses of neurons were measured in Layer 2/3 of visual and somatosensory cortices of anesthetized GCaMP6s mice in response to ICMS trains with fixed amplitude and frequency (Fixed) and three dynamic ICMS trains that increased the stimulation intensity during the onset and offset of stimulation by modulating the amplitude (DynAmp), frequency (DynFreq), or amplitude and frequency (DynBoth). ICMS was provided for either 1-s with 4-s breaks (Short) or for 30-s with 15-s breaks (Long). Results: DynAmp and DynBoth trains evoked distinct onset and offset transients in recruited neural populations, while DynFreq trains evoked population activity similar to Fixed trains. Individual neurons had heterogeneous responses primarily based on how quickly they depressed to ICMS, where neurons farther from the electrode depressed faster and a small subpopulation (1–5%) were modulated by DynFreq trains. Neurons that depressed to Short trains were also more likely to depress to Long trains, but Long trains induced more depression overall due to the increased stimulation length. Increasing the amplitude during the hold phase resulted in an increase in recruitment and intensity which resulted in more depression and reduced offset responses. Dynamic amplitude modulation reduced stimulation induced depression by 14.6 ± 0.3% for Short and 36.1 ± 0.6% for Long trains. Ideal observers were 0.031 ± 0.009 s faster for onset detection and 1.33 ± 0.21 s faster for offset detection with dynamic amplitude encoding. Conclusions: Dynamic amplitude modulation evokes distinct onset and offset transients, reduces depression of neural calcium activity, and decreases total charge injection for sensory feedback in BCIs by lowering recruitment of neurons during long maintained periods of ICMS. In contrast, dynamic frequency modulation evokes distinct onset and offset transients in a small subpopulation of neurons but also reduces depression in recruited neurons by reducing the rate of activation. 

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