Precise temperature compensation of phase in a rhythmic motor pattern
Open accessAbstract
Most animal species are cold-blooded, and their neuronal circuits must maintain function despite environmental temperature fluctuations. The central pattern generating circuits that produce rhythmic motor patterns depend on the orderly activation of circuit neurons. We describe the effects of temperature on the pyloric rhythm of the stomatogastric ganglion of the crab, Cancer borealis. The pyloric rhythm is a triphasic motor pattern in which the Pyloric Dilator (PD), Lateral Pyloric (LP), and Pyloric (PY) neurons fire in a repeating sequence. While the frequency of the pyloric rhythm increased about 4-fold (Q(10) approximately 2.3) as the temperature was shifted from 7 degrees C to 23 degrees C, the phase relationships of the PD, LP, and PY neurons showed almost perfect temperature compensation. The Q(10)'s of the input conductance, synaptic currents, transient outward current (I(A)), and the hyperpolarization-activated inward current (I(h)), all of which help determine the phase of LP neuron activity, ranged from 1.8 to 4. We studied the effects of temperature in >1,000 computational models (with different sets of maximal conductances) of a bursting neuron and the LP neuron. Many bursting models failed to monotonically increase in frequency as temperature increased. Temperature compensation of LP neuron phase was facilitated when model neurons' currents had Q(10)'s close to 2. Together, these data indicate that although diverse sets of maximal conductances may be found in identified neurons across animals, there may be strong evolutionary pressure to restrict the Q(10)'s of the processes that contribute to temperature compensation of neuronal circuits.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In initial studies of the effects of temperature on the pyloric rhythm of crabs, the rhythm increased in frequency in a permissive range, but then crashed or lost function at temperatures above 25-28°C.
“In our initial studies of the effects of temperature on the pyloric rhythm of crabs, we found that the rhythm increased in frequency in a permissive range, but then 'crashed' or lost function at temperatures above 25-28 • C [41, 65,66].”
From A feature and not a bug: Replication failures can lead to new biology (2026) · cites this paper as [41]
The Results section, “Effects of Temperature on the Pyloric Rhythm” (page unavailable), reports that the crab pyloric rhythm increased about fourfold in frequency as temperature rose from 7°C to 23°C. It does not report a crash or loss of function above 25–28°C; the biological recordings described here stop at 23°C. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
How multiple conductances determine electrophysiological properties in a multicompartment model
Taylor, A. L., Goaillard, J.-M., & Marder, E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4438-08.2009 · Cited by 202 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 48
- [1]Rosbash M 2009 The implications of multiple circadian clock origins. PLoS Biol 7 e62 doi: 10.1371/journal.pbio.1000062 19296723 PMC2656552 · DOI
- [2]Mehra A Shi M Baker C. L Colot H. V Loros J. J 2009 A role for casein kinase 2 in the mechanism underlying circadian temperature compensation. Cell 137 749 760 19450520 PMC2718715
- [3]Lenz P. H Hower A. E Hartline D. K 2005 Temperature compensation in the escape response of a marine copepod, Calanus finmarchicus (Crustacea). Biol Bull 209 75 85 16110095
- [4]Cao X. J Oertel D 2005 Temperature affects voltage-sensitive conductances differentially in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 94 821 832 15800074
- [5]Moran M. M Xu H Clapham D. E 2004 TRP ion channels in the nervous system. Curr Opin Neurobiol 14 362 369 15194117
- [6]Peloquin J. B Doering C. J Rehak R McRory J. E 2008 Temperature dependence of Cav1.4 calcium channel gating. Neuroscience 151 1066 1083 18206315
- [10]Donahue M. J Nichols A Santamaria C. A League-Pike P. E Krediet C. J 2009 Predation risk, prey abundance, and the vertical distribution of three brachyuran crabs on Gulf of Maine shores. Journal of Crustacean Biology 29 523 531
- [11]Krediet C. J Donahue M. J 2009 Growth-mortality trade-offs along a depth gradient in Cancer borealis. Journal of Experimental Marine Biology and Ecology 373 133 139
- [12]Maynard D. M Dando M. R 1974 The structure of the stomatogastric neuromuscular system in Callinectes sapidus, Homarus americanus and Panulirus argus (decapoda crustacea). Philos Trans R Soc Lond (Biol) 268 161 220 4152406
- [13]Eisen J. S Marder E 1984 A mechanism for production of phase shifts in a pattern generator. J Neurophysiol 51 1375 1393 6145759
- [14]Hartline D. K Gassie D. V Jr 1979 Pattern generation in the lobster (Panulirus) stomatogastric ganglion. I. Pyloric neuron kinetics and synaptic interactions. Biol Cybern 33 209 222 497265
- [15]Goaillard J. M Taylor A. L Schulz D. J Marder E 2009 Functional consequences of animal-to-animal variation in circuit parameters. Nat Neurosci 12 1424 1430 19838180 PMC2826985
- [16]Harris-Warrick R. M Coniglio L. M Barazangi N Guckenheimer J Gueron S 1995 Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J Neurosci 15 342 358 7823140 PMC6578330
- [17]Tierney A. J Harris-Warrick R. M 1992 Physiological role of the transient potassium current in the pyloric circuit of the lobster stomatogastric ganglion. J Neurophysiol 67 599 609 1578246
- [18]Rabbah P Nadim F 2005 Synaptic dynamics do not determine proper phase of activity in a central pattern generator. J Neurosci 25 11269 11278 16339022 PMC6725900
- [19]Bucher D Prinz A. A Marder E 2005 Animal-to-animal variability in motor pattern production in adults and during growth. J Neurosci 25 1611 1619 15716396 PMC6725924
- [20]Greenberg I Manor Y 2005 Synaptic depression in conjunction with A-current channels promote phase constancy in a rhythmic network. J Neurophysiol 93 656 677 15356180
- [21]Manor Y Bose A Booth V Nadim F 2003 Contribution of synaptic depression to phase maintenance in a model rhythmic network. J Neurophysiol 90 3513 3528 12815020
- [22]Hooper S. L 1997 Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion. J Comput Neurosci 4 191 205 9257232
- [23]Hooper S. L 1997 The pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion comprises two phase maintaining subsets. J Comput Neurosci 4 207 219 9257233
- [24]Mouser C Nadim F Bose A 2008 Maintaining phase of the crustacean tri-phasic pyloric rhythm. J Math Biol 57 161 181 18084765 PMC2475598
- [25]Liu Z Golowasch J Marder E Abbott L. F 1998 A model neuron with activity-dependent conductances regulated by multiple calcium sensors. J Neurosci 18 2309 2320 9502792 PMC6793093
- [27]Harris-Warrick R. M Coniglio L. M Levini R. M Gueron S Guckenheimer J 1995 Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. J Neurophysiol 74 1404 1420 8989381
- [28]Hartline D. K 1979 Pattern generation in the lobster (Panulirus) stomatogastric ganglion. II. Pyloric network simulation. Biol Cybern 33 223 236 227480
- [29]Rabbah P Nadim F 2007 Distinct synaptic dynamics of heterogeneous pacemaker neurons in an oscillatory network. J Neurophysiol 97 2239 2253 17202242 PMC2435166
- [30]Eisen J. S Marder E 1982 Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons. J Neurophysiol 48 1392 1415 6296329
- [31]Ayali A Harris-Warrick R. M 1999 Monoamine control of the pacemaker kernel and cycle frequency in the lobster pyloric network. J Neurosci 19 6712 6722 10415000 PMC6782821
- [32]Hooper S. L Marder E 1987 Modulation of the lobster pyloric rhythm by the peptide proctolin. J Neurosci 7 2097 2112 3612231 PMC6568943
- [33]Soto-Trevino C Rabbah P Marder E Nadim F 2005 Computational model of electrically coupled, intrinsically distinct pacemaker neurons. J Neurophysiol 94 590 604 15728775 PMC1941697
- [34]Turrigiano G. G LeMasson G Marder E 1995 Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons. J Neurosci 15 3640 3652 7538565 PMC6578228
- [35]Szabo T. M Brookings T Preuss T Faber D. S 2008 Effects of temperature acclimation on a central neural circuit and its behavioral output. J Neurophysiol 100 2997 3008 18922942 PMC3815284
- [36]Garlick K. M Robertson R. M 2007 Cytoskeletal stability and heat shock-mediated thermoprotection of central pattern generation in Locusta migratoria. Comp Biochem Physiol A Mol Integr Physiol 147 344 348 17368062
- [37]Shoemaker K. L Robertson R. M 1998 Flight motor patterns of locusts responding to thermal stimuli. Journal of Comparative Physiology A-Sensory Neural and Behavioral Physiology 183 477 488
- [39]Neumeister H Ripley B Preuss T Gilly W. F 2000 Effects of temperature on escape jetting in the squid Loligo opalescens. J Exp Biol 203 547 557 10637183
- [40]Nouvian R 2007 Temperature enhances exocytosis efficiency at the mouse inner hair cell ribbon synapse. J Physiol 584 535 542 17717016 PMC2277147
- [41]Klyachko V. A Stevens C. F 2006 Temperature-dependent shift of balance among the components of short-term plasticity in hippocampal synapses. J Neurosci 26 6945 6957 16807324 PMC6673910
- [42]Robertson R. M 1993 Effects of temperature on synaptic potentials in the locust flight system. J Neurophysiol 70 2197 2204 8120577
- [43]Heitler W. J Edwards D. H 1998 Effect of temperature on a voltage-sensitive electrical synapse in crayfish. J Exp Biol 201 503 513 9438826
- [44]Johnson B. R Peck J. H Harris-Warrick R. M 1991 Temperature sensitivity of graded synaptic transmission in the lobster stomatogastric ganglion. J Exp Biol 156 267 285 1646850
- [45]Johnson B. R Peck J. H Harris-Warrick R. M 1992 Elevated temperature alters the ionic dependence of amine-induced pacemaker activity in a conditional burster neuron. J Comp Physiol [A] 170 201 209 1583605
- [46]Zhurov Y Brezina V 2005 Temperature compensation of neuromuscular modulation in Aplysia. J Neurophysiol 94 3259 3277 15944231 PMC1564116
- [47]Nadim F Manor Y 2000 The role of short-term synaptic dynamics in motor control. Curr Opin Neurobiol 10 683 690 11240276
- [48]Bose A Manor Y Nadim F 2004 The activity phase of postsynaptic neurons in a simplified rhythmic network. J Comput Neurosci 17 245 261 15306742
- [49]Wallén P Williams T. L 1984 Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. J Physiol 347 225 239 6142945 PMC1199444
- [51]Braun G Mulloney B 1993 Cholinergic modulation of the swimmeret motor system in crayfish. J Neurophysiol 70 2391 2398 7907133
- [52]Long M. A Fee M. S 2008 Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456 189 194 19005546 PMC2723166
- [53]Schulz D. J Goaillard J. M Marder E 2006 Variable channel expression in identified single and electrically coupled neurons in different animals. Nat Neurosci 9 356 362 16444270
- [54]Schulz D. J Goaillard J. M Marder E. E 2007 Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proc Natl Acad Sci U S A 104 13187 13191 17652510 PMC1933263
Cited by
Sorted by citations
Functional segregation of cortical regions underlying speech timing and articulation
Long, M. A., Katlowitz, K. A., Svirsky, M. A., Clary, R. C., Byun, T. M., Majaj, N., Oya, H., Howard, M. A., & Greenlee, J. D. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.032 · Cited by 151 · see citing works
A biophysical perspective on the resilience of neuronal excitability across timescales
Marom, S., & Marder, E. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00730-9 · Cited by 59 · see citing works
Self-citationDegeneracy in the nervous system: From neuronal excitability to neural coding
Kamaleddin, M. A. (2022) · BioEssays · doi:10.1002/bies.202100148 · Cited by 24 · see citing works
A feature and not a bug: Replication failures can lead to new biology
Marder, E. (2026) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2026.103268
Self-citation
- Authors
- Tang, L. S., Goeritz, M. L., Caplan, J. S., Taylor, A. L., Fisek, M., & Marder, E.
- Affiliations
- Brandeis University (US)
- Corresponding author
- Marder, Eve
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-08-31
- Volume
- 8
- Issue
- 8
- Pages
- e1000469
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC2930868
- OpenAlex
- W1985995409
- Cited by
- 156
- References
- 1
- Citations by year
- 2026: 8 · 2025: 10 · 2024: 22 · 2023: 11 · 2022: 16 · 2021: 9 · 2020: 7 · 2019: 7 · 2018: 7 · 2017: 6 · 2016: 6 · 2015: 12 · 2014: 14 · 2013: 7 · 2012: 6
- FWCI
- 3.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Brandeis Institutional Repository (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (5p01ns044232-10)
- National Institute of Mental Health (MH 46742, R37MH046742, R01MH046742)
- National Institute of Neurological Disorders and Stroke (P01 NS-044232, 2P01 NS-044232)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- temperature compensation, pyloric rhythm, stomatogastric ganglion, Cancer borealis, central pattern generator, Q10, pyloric dilator neuron, lateral pyloric neuron, maximal conductance, ectotherms
- MeSH terms
- Animals, Brachyura, Motor Activity, Motor Neurons, Synaptic Transmission, Periodicity, Pylorus, Temperature, Ganglia, Invertebrate
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review