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  • 1
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 222(22), (2019): jeb212464, doi:10.1242/jeb.212464.
    Description: Escape swimming is a crucial behavior by which undulatory swimmers evade potential threats. The hydrodynamics of escape swimming have not been well studied, particularly for anguilliform swimmers, such as the sea lamprey Petromyzon marinus. For this study, we compared the kinematics and hydrodynamics of larval sea lampreys with those of lampreys accelerating from rest during escape swimming. We used experimentally derived velocity fields to calculate pressure fields and distributions of thrust and drag along the body. Lampreys initiated acceleration from rest with the formation of a high-amplitude body bend at approximately one-quarter body length posterior to the head. This deep body bend produced two high-pressure regions from which the majority of thrust for acceleration was derived. In contrast, steady swimming was characterized by shallower body bends and negative-pressure-derived thrust, which was strongest near the tail. The distinct mechanisms used for steady swimming and acceleration from rest may reflect the differing demands of the two behaviors. High-pressure-based mechanisms, such as the one used for acceleration from rest, could also be important for low-speed maneuvering during which drag-based turning mechanisms are less effective. The design of swimming robots may benefit from the incorporation of such insights from unsteady swimming.
    Description: This research was supported by grants from the National Science Foundation (UNS-1511996 and IDBR-1455471 to B.J.G., J.O.D., S.P.C. and J.H.C.). J.R.M. was funded by the Marine Biological Laboratory.
    Description: 2020-11-18
    Keywords: Petromyzon marinus ; Lamprey ; Undulatory ; Thrust ; Drag
    Repository Name: Woods Hole Open Access Server
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  • 2
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223 (2020): jeb.211276, doi: 10.1242/jeb.211276.
    Description: Previous studies have demonstrated that male European lobsters (Homarus gammarus) use chemical and visual signals as a means of intraspecific communication during agonistic encounters. In this study, we show that they also produce buzzing sounds during these encounters. This result was missed in earlier studies because low-frequency buzzing sounds are highly attenuated in tanks, and are thus difficult to detect with hydrophones. To address this issue, we designed a behavioural tank experiment using hydrophones, with accelerometers placed on the lobsters to directly detect their carapace vibrations (i.e. the sources of the buzzing sounds). While we found that both dominant and submissive individuals produced carapace vibrations during every agonistic encounter, very few of the associated buzzing sounds (15%) were recorded by the hydrophones. This difference is explained by their high attenuation in tanks. We then used the method of algorithmic complexity to analyse the carapace vibration sequences as call-and-response signals between dominant and submissive individuals. Even though some intriguing patterns appeared for closely size-matched pairs (〈5 mm carapace length difference), the results of the analysis did not permit us to infer that the processes underlying these sequences could be differentiated from random ones. Thus, such results prevented any conclusions about acoustic communication. This concurs with both the high attenuation of the buzzing sounds during the experiments and the poor understanding of acoustic perception by lobsters. New approaches that circumvent tank acoustic issues are now required to validate the existence of acoustic communication in lobsters.
    Description: This research was carried out as part of the PhD research project of Youenn Jézéquel for the Université de Bretagne Occidentale (Brest) with a grant from the French Ministry of Higher Education and Research.
    Description: 2021-02-19
    Keywords: Passive acoustics ; Accelerometer ; Buzzing sound ; Carapace vibration ; Tank ; Acoustic communication ; Dominance ; Sound attenuation
    Repository Name: Woods Hole Open Access Server
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  • 3
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology (2020): jeb.220830, doi: 10.1242/jeb.220830.
    Description: Calanoid copepods, depending on feeding strategy, have different behavioral and biological controls on their movements, thereby responding differently to environmental conditions such as changes in seawater viscosity. To understand how copepod responses to environmental conditions are mediated through physical, physiological, and/or behavioral pathways, we used high-speed microvideography to compare two copepod species, Acartia hudsonica and Parvocalanus crassirostris, under different temperature, viscosity, and dietary conditions. Acartia hudsonica exhibited “sink and wait” feeding behavior and typically responded to changes in seawater viscosity; increased seawater viscosity reduced particle-capture behavior and decreased the size of the feeding current. In contrast, P. crassirostris continuously swam and did not show any behavioral or physical responses to changes in viscosity. Both species showed a physiological response to temperature, with reduced appendage beating frequency at cold temperatures, but this did not generally translate into effects on swimming speed, feeding flux, or active time. Both copepod species swam slower when feeding on diatom rather than dinoflagellate prey, showing that prey type mediates copepod behavior. These results differentiate species-specific behaviors and responses to environmental conditions, which may lead to better understanding of niche separation and latitudinal patterns in copepod feeding and movement strategies.
    Description: This study was supported by the National Science Foundation [OCE1634024 to N.F.; OCE-1433979 and OCE-1559062 to H.J.]; and by Stony Brook University [Graduate Council Fellowship and Turner Fellowship to A.S.T].
    Description: 2021-06-11
    Keywords: Copepods ; Zooplankton ; Seawater viscosity ; Feeding mechanism ; Micro-particle tracking velocimetry (µPTV)
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  • 4
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223(11), (2020): jeb224915, doi: 10.1242/jeb.224915.
    Description: Costs of sound production have been investigated only sparsely incetaceans, despite recent efforts to understand how increasinganthropogenic noise affects these animals that rely extensively onsound for communication and foraging. Theoretical estimates suggestthat metabolic costs of whistling for bottlenose dolphins should be〈0.54% of resting metabolic rate (RMR) (Jensen et al., 2012),whereas empirical studies of a single whistling dolphin surprisinglyclaimed that sound production costs were around 20% of RMR (Holtet al., 2015; Noren et al., 2013). Addressing this discrepancy, wefound that costs of whistling were significantly less than 20% RMRand not statistically different from theoretical estimates (Pedersenet al., 2020). In their correspondence, Noren et al., 2020 argue thatthey did not claim whistling was‘costly’and questioned aspects ofour methods, and we address these points here.
    Description: 2021-06-08
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  • 5
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology (2020): jeb.219683, doi: 10.1242/jeb.219683.
    Description: Black sea bass (Centropristis striata) is an important fish species in both commercial and recreational fisheries of southern New England and the mid-Atlantic Bight. Due to the intense urbanization of these waters, this species is subject to a wide range of anthropogenic noise pollution. Concerns that C. striata are negatively affected by pile driving and construction noise predominate in areas earmarked for energy development. However, as yet, the hearing range of C. striata is unknown, making it hard to evaluate potential risks. This study is a first step in understanding the effects of anthropogenic noise on C. striata by determining the auditory bandwidth and thresholds of this species using auditory evoked potentials (AEPs), creating pressure and acceleration audiograms. These physiological tests were conducted on wild-caught C. striata in three size/age categories. Results showed that juvenile C. striata significantly had the lowest thresholds, with hearing sensitivity decreasing in the larger size classes. Furthermore, Centropristis striata has fairly sensitive hearing relative to other related species. Preliminary investigations into the mechanisms of their hearing ability were undertaken with gross dissections and an opportunistic micro computed tomography image to address the auditory structures including otoliths and swimbladder morphology. Crucially, the hearing range of C. striata, and their most sensitive frequencies, directly overlap with high-amplitude anthropogenic noise pollution such as shipping and underwater construction.
    Description: This work was funded by the Bureau of Ocean Energy Management Environmental Studies Program through Interagency Agreement Number M17PG00029 with the U.S. Department of Commerce, National Oceanic and Atmospheric Administration.
    Description: 2021-05-27
    Keywords: Centropristis striata ; Fish hearing ; Pile driving ; Anthropogenic sound ; AEP
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  • 6
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 222 (2019): jeb.216606, doi: 10.1242/jeb.216606
    Description: Anthropogenic underwater noise has increased over the past century, raising concern about the impact on cetaceans that rely on sound for communication, navigation and locating prey and predators. Many terrestrial animals increase the amplitude of their acoustic signals to partially compensate for the masking effect of noise (the Lombard response), but it has been suggested that cetaceans almost fully compensate with amplitude adjustments for increasing noise levels. Here, we used sound-recording DTAGs on pairs of free-ranging common bottlenose dolphins (Tursiops truncatus) to test (i) whether dolphins increase signal amplitude to compensate for increasing ambient noise and (ii) whether adjustments are identical for different signal types. We present evidence of a Lombard response in the range 0.1–0.3 dB per 1 dB increase in ambient noise, which is similar to that of terrestrial animals, but much lower than the response reported for other cetaceans. We found that signature whistles tended to be louder and with a lower degree of amplitude adjustment to noise compared with non-signature whistles, suggesting that signature whistles may be selected for higher output levels and may have a smaller scope for amplitude adjustment to noise. The consequence of the limited degree of vocal amplitude compensation is a loss of active space during periods of increased noise, with potential consequences for group cohesion, conspecific encounter rates and mate attraction.
    Description: Fieldwork in Sarasota was funded by the Grossman Foundation, the Office of Naval Research, and Woods Hole Oceanographic Institution. Health assessments were funded by Dolphin Quest, Inc. I.M.K. received support from the Danish Acoustical Society (Dansk Akustisk Selskab). P.L.T. received funding from the University of St Andrews, the Office of Naval Research (N00014-19-1-2560) and the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland). F.H.J. was supported by the Office of Naval Research (N00014-1410410) and an AIAS-COFUND fellowship from Aarhus Institute of Advanced Studies under the FP7-PEOPLE programme of the EU (agreement no. 609033). All support is gratefully acknowledged.
    Description: 2020-11-08
    Keywords: Cetacean ; Signature whistle ; Communication ; Anthropogenic noise ; Masking ; Lombard response
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  • 7
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223(1), (2019): jeb.212498, doi: 10.1242/jeb.212498.
    Description: Toothed whales depend on sound for communication and foraging, making them potentially vulnerable to acoustic masking from increasing anthropogenic noise. Masking effects may be ameliorated by higher amplitudes or rates of calling, but such acoustic compensation mechanisms may incur energetic costs if sound production is expensive. The costs of whistling in bottlenose dolphins (Tursiops truncatus) have been reported to be much higher (20% of resting metabolic rate, RMR) than theoretical predictions (0.5–1% of RMR). Here, we address this dichotomy by measuring the change in the resting O2 consumption rate (V̇O2), a proxy for RMR, in three post-absorptive bottlenose dolphins during whistling and silent trials, concurrent with simultaneous measurement of acoustic output using a calibrated hydrophone array. The experimental protocol consisted of a 2-min baseline period to establish RMR, followed by a 2-min voluntary resting surface apnea, with or without whistling as cued by the trainers, and then a 5-min resting period to measure recovery costs. Daily fluctuations in V̇O2 were accounted for by subtracting the baseline RMR from the recovery costs to estimate the cost of apnea with and without whistles relative to RMR. Analysis of 52 sessions containing 1162 whistles showed that whistling did not increase metabolic cost (P〉0.1, +4.2±6.9%) as compared with control trials (−0.5±5.9%; means±s.e.m.). Thus, we reject the hypothesis that whistling is costly for bottlenose dolphins, and conclude that vocal adjustments such as the Lombard response to noise do not represent large direct energetic costs for communicating toothed whales.
    Description: M.P.B. received financial support from a Company of Biologists JEB travel fellowship JEBTF181150, and a grant from the Danish Acoustical Society. F.H.J. was supported by an AIAS-COFUND fellowship from Aarhus Institute of Advanced Studies under the FP7 program of the EU (agreement no. 609033). P.T.M. and recording equipment were funded by a large frame grant from Danish Council for Independent Research | Natural Sciences (Natur og Univers, Det Frie Forskningsråd). A.F. was supported by Fundación Oceanogràfic de la Comunitat Valenciana and Global Diving Research.
    Description: 2020-12-03
    Keywords: Respiratory physiology ; Sound production ; Acoustic communication ; Underwater noise ; Vocal modifications ; Toothed whales
    Repository Name: Woods Hole Open Access Server
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  • 8
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223 (2019): jeb.216283, doi: 10.1242/jeb.216283.
    Description: Toothed whales have evolved flexible biosonar systems to find, track and capture prey in diverse habitats. Delphinids, phocoenids and iniids adjust inter-click intervals and source levels gradually while approaching prey. In contrast, deep-diving beaked and sperm whales maintain relatively constant inter-click intervals and apparent output levels during the approach followed by a rapid transition into the foraging buzz, presumably to maintain a long-range acoustic scene in a multi-target environment. However, it remains unknown whether this rapid biosonar adjustment strategy is shared by delphinids foraging in deep waters. To test this, we investigated biosonar adjustments of a deep-diving delphinid, the Risso's dolphin (Grampus griseus). We analyzed inter-click interval and apparent output level adjustments recorded from sound recording tags to quantify in situ sensory adjustment during prey capture attempts. Risso's dolphins did not follow typical (20logR) biosonar adjustment patterns seen in shallow-water species, but instead maintained stable repetition rates and output levels up to the foraging buzz. Our results suggest that maintaining a long-range acoustic scene to exploit complex, multi-target prey layers is a common strategy amongst deep-diving toothed whales. Risso's dolphins transitioned rapidly into the foraging buzz just like beaked whales during most foraging attempts, but employed a more gradual biosonar adjustment in a subset (19%) of prey approaches. These were characterized by higher speeds and minimum specific acceleration, indicating higher prey capture efforts associated with evasive prey. Thus, tracking and capturing evasive prey using biosonar may require a more gradual switch between multi-target echolocation and single-target tracking.
    Description: F.H.J. was supported by an AIAS-COFUND fellowship from Aarhus Institute of Advanced Studies under the FP7 program of the EU Seventh Framework Programme (agreement no. 609033). F.V. was supported by the Office of Naval Research (ONR) (grants N00014-15-1-2341 and N00014-17-1-2715) and the Dutch Research Council (award number 016.Veni.181.086). P.L.T. was supported by ONR (grants N00014-15-1-2553 and N00014-18-1-2062) and acknowledges the support of the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) in the completion of this study. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.
    Description: 2020-12-10
    Keywords: Echolocation ; Sensory ecology ; Mesopelagic foraging ; Deep-water environment ; Biosonar strategies ; Gain control
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  • 9
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223(3), (2019): jeb.218081, doi: 10.1242/jeb.218081.
    Description: An important aspect of the performance of many fast muscle fiber types is rapid excitation. Previous research on the cross-striated muscle fibers responsible for the rapid tentacle strike in squid has revealed the specializations responsible for high shortening velocity, but little is known about excitation of these fibers. Conventional whole-cell patch recordings were made from tentacle fibers and the slower obliquely striated muscle fibers of the arms. The fast-contracting tentacle fibers show an approximately 10-fold greater sodium conductance than that of the arm fibers and, unlike the arm fibers, the tentacle muscle fibers produce action potentials. In situ hybridization using an antisense probe to the voltage-dependent sodium channel present in this squid genus shows prominent expression of sodium channel mRNA in tentacle fibers but undetectable expression in arm fibers. Production of action potentials by tentacle muscle fibers and their absence in arm fibers is likely responsible for the previously reported greater twitch–tetanus ratio in the tentacle versus the arm fibers. During the rapid tentacle strike, a few closely spaced action potentials would result in maximal activation of transverse tentacle muscle. Activation of the slower transverse muscle fibers in the arms would require summation of excitatory postsynaptic potentials over a longer time, allowing the precise modulation of force required for supporting slower movements of the arms.
    Description: This work was supported by the National Science Foundation (IOS 1557754 to W.F.G. and IOS 0951067 to W.M.K.).
    Description: 2021-01-03
    Keywords: Calcium current ; Cephalopod muscle ; Current clamp ; Patch clamp ; Sodium current ; Voltage clamp
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  • 10
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hahn, M. E., & Sadler, K. C. Casting a wide net: use of diverse model organisms to advance toxicology. Disease Models & Mechanisms, 13, (2020): dmm.043844, doi: 10.1242/dmm.043844.
    Description: Toxicology – the study of how chemicals interact with biological systems – has clear relevance to human health and disease. Persistent exposure to natural and synthetic chemicals is an unavoidable part of living on our planet; yet, we understand very little about the effects of exposure to the vast majority of chemicals. While epidemiological studies can provide strong statistical inference linking chemical exposure to disease, research in model systems is essential to elucidate the mechanisms of action and to predict outcomes. Most research in toxicology utilizes a handful of mammalian models that represent a few distinct branches of the evolutionary tree. This narrow focus constrains the understanding of chemical-induced disease processes and systems that have evolved in response to exposures. We advocate for casting a wider net in environmental toxicology research to utilize diverse model systems, including zebrafish, and perform more mechanistic studies of cellular responses to chemical exposures to shift the perception of toxicology as an applied science to that of a basic science. This more-inclusive perspective will enrich the field and should remain central to research on chemical-induced disease.
    Description: K.C.S. acknowledges support from the National Institutes of Health (NIH)(5R01AA018886). M.E.H. acknowledges support from the National Institute ofEnvironmental Health Sciences (NIEHS) through the Boston University SuperfundResearch Program (P42ES007381) and the Woods Hole Center for Oceans andHuman Health (NIEHS grant P01ES028938 and National Science Foundation grantOCE-1840381).
    Keywords: Animal models ; Toxicants ; Toxicology ; Zebrafish
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  • 11
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223 (2020): jeb217885, doi:10.1242/jeb.217885.
    Description: Assessment of the compressibility of marine mammal airways at depth is crucial to understanding vital physiological processes such as gas exchange during diving. Very few studies have directly assessed changes in cetacean and pinniped tracheobronchial shape, and none have quantified changes in volume with increasing pressure. A harbor seal, gray seal, harp seal, harbor porpoise and common dolphin were imaged promptly post mortem via computed tomography in a radiolucent hyperbaric chamber. Volume reconstructions were performed of segments of the trachea and bronchi of the pinnipeds and bronchi of the cetaceans for each pressure treatment. All specimens examined demonstrated significant decreases in airway volume with increasing pressure, with those of the harbor seal and common dolphin nearing complete collapse at the highest pressures. The common dolphin bronchi demonstrated distinctly different compression dynamics between 50% and 100% lung inflation treatments, indicating the importance of air in maintaining patent airways, and collapse occurred caudally to cranially in the 50% treatment. Dynamics of the harbor seal and gray seal airways indicated that the trachea was less compliant than the bronchi. These findings indicate potential species-specific variability in airway compliance, and cessation of gas exchange may occur at greater depths than those predicted in models assuming rigid airways. This may potentially increase the likelihood of decompression sickness in these animals during diving.
    Description: This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
    Description: 2021-02-10
    Keywords: Computed tomography ; Marine mammal ; Trachea ; Bronchi ; Airway compression
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  • 12
    Publication Date: 2022-05-26
    Description: Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223 (2020): jeb.204438, doi:10.1242/jeb.204438.
    Description: An animal's own movement exerts a profound impact on sensory input to its nervous system. Peripheral sensory receptors do not distinguish externally generated stimuli from stimuli generated by an animal's own behavior (reafference) – although the animal often must. One way that nervous systems can solve this problem is to provide movement-related signals (copies of motor commands and sensory feedback) to sensory systems, which can then be used to generate predictions that oppose or cancel out sensory responses to reafference. Here, we studied the use of movement-related signals to generate sensory predictions in the lateral line medial octavolateralis nucleus (MON) of the little skate. In the MON, mechanoreceptive afferents synapse on output neurons that also receive movement-related signals from central sources, via a granule cell parallel fiber system. This parallel fiber system organization is characteristic of a set of so-called cerebellum-like structures. Cerebellum-like structures have been shown to support predictive cancellation of reafference in the electrosensory systems of fish and the auditory system of mice. Here, we provide evidence that the parallel fiber system in the MON can generate predictions that are negative images of (and therefore cancel) sensory input associated with respiratory and fin movements. The MON, found in most aquatic vertebrates, is probably one of the most primitive cerebellum-like structures and a starting point for cerebellar evolution. The results of this study contribute to a growing body of work that uses an evolutionary perspective on the vertebrate cerebellum to understand its functional diversity in animal behavior.
    Description: This work was supported by National Science Foundation (NSF) and Wesleyan University grants to D.B. Funding for K.E.P. while performing these experiments came in part from a grant from the HHMI Hughes V award for undergraduate education to Wesleyan University (52005211) in the form of a summer research fellowship. A.K. was supported in part by an NSF-REU Award (1659604) and a Wesleyan University Summer Research Fellowship. K.E.P. is currently supported through funding from the Simons Society of Fellows as a Junior Fellow.
    Description: 2021-01-17
    Keywords: Cerebellum-like ; Mechanosensory lateral line ; Predictive cancellation ; Reafference ; Elasmobranch ; Sensory system
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