How animals respond to repeatedly applied stimuli, and how animals respond to mechanical stimuli in particular, are important questions in behavioral neuroscience. We study adaptation to repeated mechanical agitation using theDrosophilalarva. Vertical vibration stimuli elicit a discrete set of responses in crawling larvae: continuation, pause, turn, and reversal. Through high-throughput larva tracking, we characterize how the likelihood of each response depends on vibration intensity and on the timing of repeated vibration pulses. By examining transitions between behavioral states at the population and individual levels, we investigate how the animals habituate to the stimulus patterns. We identify time constants associated with desensitization to prolonged vibration, with re-sensitization during removal of a stimulus, and additional layers of habituation that operate in the overall response. Known memory-deficient mutants exhibit distinct behavior profiles and habituation time constants. An analogous simple electrical circuit suggests possible neural and molecular processes behind adaptive behavior.
more »
« less
Unbiased analysis of C. elegans behavior reveals the use of distinct turning strategies during magnetic Orientation
Abstract To successfully navigate their surroundings, animals detect and orient to environmental stimuli possessing unique physical properties. Most animals can derive directional information from spatial or temporal changes in stimulus intensity (e.g. chemo- and thermo-taxis). However, some biologically relevant stimuli have constant intensity at most organismal scales. The gravitational and magnetic fields of the earth are examples of uniform stimuli that remain constant at most relevant scales. While devoid of information associated with intensity changes, the vectorial nature of these fields intrinsically encodes directional information. While much is known about behavioral strategies that exploit changes in stimulus intensity (gradients), less is understood about orientation to uniform stimuli. Nowhere is this truer than with magnetic orientation. While many organisms are known to orient to the magnetic field of the earth, how these animals extract information from the earth’s magnetic field remains unresolved. Here we use the nematodeC. elegansto investigate behavioral strategies for orientation to magnetic fields, and compare our findings to the better characterized chemical and thermal orientation strategies. We used an unbiased cluster analysis to categorize, quantify, and compare behavioral components underlying different orientation strategies as a way to quantify and compare animal orientation to distinct stimuli. We find that in the presence of an earth-like magnetic field, worms perform acute angle turns (140-171°) that significantly improved their alignment with the direction of an imposed magnetic vector. In contrast, animals performed high amplitude turns (46-82°) that significantly increased alignment of their trajectory with the preferred migratory angle. We conclude thatC. elegansorients to earth-strength magnetic fields using two independent behavioral strategies, in contrast to orientation strategies to graded stimuli. Understanding howC. elegansdetects and orients to magnetic fields will provide useful insight into how many species across taxa accomplish this fascinating sensory feat.
more »
« less
- Award ID(s):
- 1818140
- PAR ID:
- 10554260
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Sung, Baeckkyoung (Ed.)Collective response to external directional cues like electric fields helps guide tissue development, regeneration, and wound healing. In this study we focus on the impact of anisotropy in cell shape and local cell alignment on the collective response to electric fields. We model elongated cells that have a different accuracy sensing the field depending on their orientation with respect to the field. With this framework, we assume cells are better sensors if they can align their long axes perpendicular to the field. Elongated cells often line up with their long axes in the same direction — “nematic order” – does a nematic cell-cell interaction allow groups of cells to share information about their orientation to sense fields more accurately? We use simulations of a simple model to show that if cells orient themselves perpendicular to their average velocity, alignment of a cell’s long axis to its nearest neighbors’ orientation can in some circumstances enhance the directional response to electric fields. We also show that cell-cell adhesion modulates the accuracy of cells in the group.more » « less
-
Sengupta, Piali (Ed.)We present a high-throughput optogenetic illumination system capable of simultaneous closed-loop light delivery to specified targets in populations of moving Caenorhabditis elegans . The instrument addresses three technical challenges: It delivers targeted illumination to specified regions of the animal’s body such as its head or tail; it automatically delivers stimuli triggered upon the animal’s behavior; and it achieves high throughput by targeting many animals simultaneously. The instrument was used to optogenetically probe the animal’s behavioral response to competing mechanosensory stimuli in the the anterior and posterior gentle touch receptor neurons. Responses to more than 43,418 stimulus events from a range of anterior–posterior intensity combinations were measured. The animal’s probability of sprinting forward in response to a mechanosensory stimulus depended on both the anterior and posterior stimulation intensity, while the probability of reversing depended primarily on the anterior stimulation intensity. We also probed the animal’s response to mechanosensory stimulation during the onset of turning, a relatively rare behavioral event, by delivering stimuli automatically when the animal began to turn. Using this closed-loop approach, over 9,700 stimulus events were delivered during turning onset at a rate of 9.2 events per worm hour, a greater than 25-fold increase in throughput compared to previous investigations. These measurements validate with greater statistical power previous findings that turning acts to gate mechanosensory evoked reversals. Compared to previous approaches, the current system offers targeted optogenetic stimulation to specific body regions or behaviors with many fold increases in throughput to better constrain quantitative models of sensorimotor processing.more » « less
-
Inhibitory feedback from the motor circuit gates mechanosensory processing in Caenorhabditis elegansSengupta, Piali (Ed.)Animals must integrate sensory cues with their current behavioral context to generate a suitable response. How this integration occurs is poorly understood. Previously, we developed high-throughput methods to probe neural activity in populations ofCaenorhabditis elegansand discovered that the animal’s mechanosensory processing is rapidly modulated by the animal’s locomotion. Specifically, we found that when the worm turns it suppresses its mechanosensory-evoked reversal response. Here, we report thatC.elegansuse inhibitory feedback from turning-associated neurons to provide this rapid modulation of mechanosensory processing. By performing high-throughput optogenetic perturbations triggered on behavior, we show that turning-associated neurons SAA, RIV, and/or SMB suppress mechanosensory-evoked reversals during turns. We find that activation of the gentle-touch mechanosensory neurons or of any of the interneurons AIZ, RIM, AIB, and AVE during a turn is less likely to evoke a reversal than activation during forward movement. Inhibiting neurons SAA, RIV, and SMB during a turn restores the likelihood with which mechanosensory activation evokes reversals. Separately, activation of premotor interneuron AVA evokes reversals regardless of whether the animal is turning or moving forward. We therefore propose that inhibitory signals from SAA, RIV, and/or SMB gate mechanosensory signals upstream of neuron AVA. We conclude thatC.elegansrely on inhibitory feedback from the motor circuit to modulate its response to sensory stimuli on fast timescales. This need for motor signals in sensory processing may explain the ubiquity in many organisms of motor-related neural activity patterns seen across the brain, including in sensory processing areas.more » « less
-
Life on Earth evolved under a specific set of environmental conditions, including consistent gravitational and magnetic fields. However, planned human missions to Mars in the coming decades will expose terrestrial organisms to radically different conditions, with Martian gravity being approximately 38% of Earth's and a significantly reduced magnetic field. Understanding the combined effects of these factors is crucial, as they may impact biological systems that evolved under different conditions. In this study, we investigated the effects of simulated Martian gravity and hypomagnetic fields on the nematode Caenorhabditis elegans across six generations. We used an integrated experimental setup consisting of clinostats to mimic the reduced Martian gravity, and Merritt coil magnetic cages to model the decreased Martian magnetic fields. We assessed behavioral, morphological, and physiological responses of C. elegans. High-throughput automated assays revealed significant reductions in motor output and morphological dimensions for animals in the Mars treatment compared to matched earth-like controls. We assessed neurological function by means of chemotaxis assays and found a progressive decline in performance for worms raised under the Martian paradigm compared to Earth controls. Our results show that worms grown under Martian-like conditions exhibit progressive physiological alterations across generations, suggesting that the unique environment of Mars might pose challenges to biological function and adaptation. These findings contribute to understanding how living organisms may respond to the combined effects of reduced gravity and hypomagnetic fields, providing insights relevant for future human exploration and potential colonization of Mars.more » « less
An official website of the United States government

