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Neural mechanisms potentially contributing to the intersegmental phase lag in lamprey I.: Segmental oscillations dependent on reciprocal inhibition
KTH, Superseded Departments, Numerical Analysis and Computer Science, NADA.ORCID iD: 0000-0002-0550-0739
KTH, Superseded Departments, Numerical Analysis and Computer Science, NADA.ORCID iD: 0000-0002-2358-7815
1999 (English)In: Biological Cybernetics, ISSN 0340-1200, E-ISSN 1432-0770, Vol. 81, no 4, 317-330 p.Article in journal (Refereed) Published
Abstract [en]

Factors contributing to the production of a phase lag along chains of oscillatory networks consisting of Hodgkin-Huxley type neurons are analyzed by means of simulations. Simplified network configurations are explored consisting of the basic building blocks of the spinal central pattern generator (CPG) generating swimming in the lamprey. It consists of reciprocally coupled crossed inhibitory C interneurons and ipsilateral excitatory E interneurons that activate C neurons and other E neurons. Oscillatory activity in the model network can, in the simplest case, be produced by a pair of reciprocally coupled C interneurons oscillating through an escape mechanism. Different levels of tonic excitation drive the network over a wide burst frequency range. In this type of network, powerful frequency-regulating factors are the effective inhibition produced by the active side, in combination with the tendency of the inactive side to escape from the inhibition. These two mechanisms can be affected by several factors, e.g. spike frequency adaptation (calcium-dependent K+ channels): N-methyl-D-aspartate membrane properties as well as presence of low-voltage activated calcium channels. A rostrocaudal phase lag can be produced either by extending the contralateral inhibitory projections or the ipsilateral excitatory projections relatively more in the caudal than the rostral direction, since both an increased inhibition and a phasic excitation slow down the receiving network. The phase lag becomes decreased if the length of the intersegmental projections is increased or if the projections are extended symmetrically in both the rostral and the caudal directions. The simulations indicate that the conditions in the ends of an oscillator chain may significantly affect sign, magnitude and constancy of the phase lag. Also, with short and relatively weak intersegmental connections, the network remains robust against perturbations as well as intrinsic frequency differences along the chain. The phase lag (percentage of cycle duration) increases, however, with burst frequency also when the coupling strength is comparatively weak. The results are discussed and compared with previous "phase pulling" models as well as relaxation oscillators.

Place, publisher, year, edition, pages
1999. Vol. 81, no 4, 317-330 p.
Keyword [en]
COMPUTER-BASED MODEL, SPINAL-CORD, FICTIVE LOCOMOTION, REALISTIC SIMULATIONS, COUPLED OSCILLATORS, MEMBRANE-PROPERTIES, PATTERN GENERATOR, NETWORK MODEL, LOW-VOLTAGE, NEURONS
National Category
Engineering and Technology
Identifiers
URN: urn:nbn:se:kth:diva-13367DOI: 10.1007/s004220050565ISI: 000083208800004OAI: oai:DiVA.org:kth-13367DiVA: diva2:324694
Note
QC 20100616Available from: 2010-06-16 Created: 2010-06-16 Last updated: 2017-12-12Bibliographically approved
In thesis
1. Modeling of bursting mechanisms and coordination in a spinal central pattern generator
Open this publication in new window or tab >>Modeling of bursting mechanisms and coordination in a spinal central pattern generator
1998 (English)Doctoral thesis, comprehensive summary (Other scientific)
Abstract [en]

Mechanisms underlying lotal bursting as well as coordinationbetween different levels of a spinal CPG generating locomotionhave been investigated using computer simulations. A"primitive" jawless vertebrate, the lamprey, is used a.s aprototype model. Most simulations have been conducted using abiophysical neu ron model built on the Hodgkin-Huxley formalismand equipped with Nu+, K+,Ca²+, Kca, LVACa²+ and NMDA activated channels. Inhibitory andexcitatory AMPA/kainate and NMDA synapses are modeled as timedependent conductances with appropriate reversal potentials.For tomparison, Morris-Letar oscillators as well as adaptingleaky integrator-like units are also used.

The basic identified building blocks of the CPG, generatingalternating left right burst activity, tonsist of ipsilaterallyprojecting excitatory neurons (E) and contralaterallyprojecting inhibitory neurons (C). The model neurons are connected in the same way ss has been established experimentally.Sinte several complementary mechanisms may play a role, thepotential of two different neural mechanisms have been exploredwhich can provide burst activity at the segmen tal level, andintersegmental coordination. When alternating left-rightactivity is produced through an escape-like mechanism the quietside is able to become ac tive despite ongoing inhibition fromthe contralateral side. Reciprocal inhibition is then a crucialburst terminating factor. Burst frequency is strongly affectedby the effective inhibition and the drive to escape fromongoing inhibition. Several factors influence this process. Kcacurrents control spike frequency on the active sideand also a post-burst hyperpolarization on the inactive side.Postin hibitory rebound properties, carried by e.g. low voltageactivatedCa²+ currents further can promote escape. Phasicipsilateral excitation and NMDA membrane properties stabilizethe rhythm, especially in the lower frequency range. Severalexperimental observations can be explained based on the effectthese different factors have on effective inhibition andtendency for escape.

Bursting can, however, also be produced by a networkdeprived of inhibition, showing that powerful burst terminatingmechanisms not requiring inhibition exist. In the model withbiophysically detailed neurons such a mechanism could beactivation ofKcacurrents due to accumulation ofCa²+ during the active phase. As shown innon-spiking, as well as biophysically detailed models, aconstant burst proportion over a wide frequency range can beachieved by modulation of the rel ative strength of adaptationin such networks. The left-right inhibition causes left-rightalternation but may not affect the frequency of bursting.

When both types of lotal oscillatory networks are extendedlongitudinally, a rostral to caudal phase delay is producedwhen caudal projections are extended further than the rostralenes. However, the excitatory versus inhibitory projec tionsmay have different roles in the two alternative models. Thisrelative phase delay expressed as % of cycle duration,increases in general with frequency. The simulations suggestthat the conditions at the ends of the simulated chain arecritical for the resulting phase lag. The capability ofbuffering against frequency variations and rapid adjustmentsfollowing perturbations is discussed and com pared with chainsof relaxation oscillators and phase-coupled oscillators.

Place, publisher, year, edition, pages
Stockholm: KTH, 1998. 82 p.
Series
Trita-NA, ISSN 0348-2952 ; 98:10
Keyword
adaptation, central pattern generator, computer simulation, inter segmental coordination, lamprey, locomotion, neural network, rhythmogenesis
National Category
Engineering and Technology
Identifiers
urn:nbn:se:kth:diva-2673 (URN)91-7170-255-5 (ISBN)
Public defence
1998-06-16, 00:00
Note
QC 20100616Available from: 2000-01-01 Created: 2000-01-01 Last updated: 2010-06-16Bibliographically approved

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