Abstract.
The information transmission properties of ensembles of MSs and the effect of the gamma system on these properties were studied. Three converging lines of research were taken: (1) the development of information theoretic estimation tools, and the formulation of an “operational” interpretation for the information rate; (2) animal experiments in which the mutual information rate was estimated and the effect of the gamma system was quantified; (3) simulation of a muscle spindle model with gamma activation in order to corroborate the results of the animal experiments. The main hypothesis was that the gamma system will enhance information theoretic measures that quantify the quality of the sensory neural channel comprised from an ensemble of primary muscle spindle afferents. A random stimulus was applied to a muscle in the hind limb of a cat, while spike trains from several primary MS afferents were recorded simultaneously. The stimulus was administered twice, with an operative and a disconnected gamma system. The mutual information rate between the stimulus and spike trains, as well as other information theoretic measures, was estimated. The information rate of ensembles of MSs increased with increasing ensemble size. However, with an operative gamma system the “ensemble effect ” was much higher. In addition, the ensemble effect was influenced by the stimulus spectrum. A muscle spindle population model with gamma activation was simulated with stimuli that were identical to that of the animal experiments. The simulation results supported the experimental results and corroborated the main hypothesis. The results indicate that the gamma system has an important role in enhancing information transmission from ensembles of MSs to the spinal cord.
Similar content being viewed by others
References
RW Banks M Hulliger KA Scheepstra E Otten (1997) ArticleTitlePacemaker activity in a sensory ending with multiple encoding sites: The cat muscle spindle primary ending J Physiol (Lond) 498 177–199 Occurrence Handle1:CAS:528:DyaK2sXmslKltQ%3D%3D
D Barker RW Banks (1994) The muscle spindle AG Engel C Franzini-Armstrong (Eds) Myology McGraw Hill New York 333–360
M Bergenheim H Johansson J Pedersen (1995) ArticleTitleThe role of the γ-system for improving information transmission in populations of ia afferents Neurosci Res 23 207–215 Occurrence Handle1:STN:280:BymC3c%2FltFw%3D Occurrence Handle8532217
W Bialek F Rieke R Ruyter Ssteveninck Particlede van D Warland (1991) ArticleTitleReading a neural code Science 252 1854–1857 Occurrence Handle1:STN:280:By6B1cbhsVE%3D Occurrence Handle2063199
RW Carr JE Gregory U Proske (1998) ArticleTitleSummation of responses of cat muscle spindles to combined static and dynamic fusimotor stimulation Brain Res 800 97–104 Occurrence Handle1:CAS:528:DyaK1cXksVyqsrk%3D Occurrence Handle9685596
TM Cover JA Thomas (1990) Elements of information theory Wiley New York
RR Ruyter Steveninck Particlede van GD Lewen SP Strong R Koberle W Bialek (1997) ArticleTitleReproducibility and variability in neural spike trains Science 275 1805–1808 Occurrence Handle9065407
M Djupsjöbacka H Johansson M Bergenheim U Sandström (1994) ArticleTitleA multichannel hook electrode for simultaneous recording of up to 12 nerve filaments J Neurosci Methods 52 69–72 Occurrence Handle8090020
B Efron R Tibshirani (1993) An introduction to the bootstrap Chapman & Hall New York
JB Fallon RW Carr JE Gregory U Proske (2001) ArticleTitleSumming responses of cat soleus muscle spindles to combined static and dynamic fusimotor stimulation Brain Res 888 348–355 Occurrence Handle1:CAS:528:DC%2BD3MXitl2iug%3D%3D Occurrence Handle11150497
Farach M, Noordewier M, Savari S, Shepp L, Wyner A, Ziv J (1995) On the entropy of DNA: Algorithms and measurements based on memory and rapid convergence. In: Proceedings in 1995 symposium on discrete algorithms, pp 48–57
RG Gallager (1968) Information theory and reliable communication Wiley New York
Y Hershkovits J Ziv (1998) ArticleTitleOn sliding-window universal data compression with limited memory IEEE Trans Inform Theory 44 66–78
M Hulliger (1984) ArticleTitleThe mammalian muscle spindle and its central control Rev Physiol Biochem Pharmacol 101 1–110 Occurrence Handle1:STN:280:BiqC3Mvos1I%3D Occurrence Handle6240757
CC Hunt (1954) ArticleTitleRelation of function to diameter in afferent fibers of muscle nerves J Gen Physiol 38 117–131 Occurrence Handle1:STN:280:CyqD3czovF0%3D Occurrence Handle13192320
CC Hunt SW Kuffler (1951) ArticleTitleStretch receptor discharges during muscle contraction J Physiol (Lond) 113 298–315 Occurrence Handle1:STN:280:Cy6D283jt1I%3D
GF Inbar J Madrid P Rudomin (1979) ArticleTitleThe influence of the gamma system on cross-correlated activity of ia muscle spindles and its relation to information transmission Neurosci Lett 13 73–78 Occurrence Handle1:STN:280:CSaB383ltVc%3D Occurrence Handle156885
C Koch (1999) Biophysics of computation: information processing in single neurons Oxford Academic Press New York
I Kontoyiannis P Algoet YM Suhov AJ Wyner (1998) ArticleTitleNon-parametric entropy estimation for stationary processes and random fields, with applications to english text IEEE Trans Inform Theory 44 1319–1327
M London A Schreibman M Häusser ME Larkum I Segev (2002) ArticleTitleThe information efficacy of a synapse Nature Neurosci 5 332–340 Occurrence Handle1:CAS:528:DC%2BD38Xis1Kis7Y%3D Occurrence Handle11896396
PHC Matthews (1933) ArticleTitleNerve endings in mammalian muscle J Physiol (Lond) 78 1–53
TA McMahon (1984) Muscles,reflexes,and locomotion Princeton University Press Princeton
DT McRuer RE Magdaleno GP Moore (1968) ArticleTitleA neuromascular actuation system model IEEE Trans Man Mach Syst 9 61–71
P Milgram GF Inbar (1976) ArticleTitleDistortion suppression in neuromascular information transmission due to interchannel dispertion in muscle spindle firing thresholds IEEE Trans BioMed Eng 23 1–15 Occurrence Handle1:STN:280:CSmD28jmtlw%3D Occurrence Handle172431
D Ornstein B Weiss (1993) ArticleTitleEntropy and data compression schemes IEEE Trans Inform Theory 39 78–83
E Otten M Hulliger KA Scheepstra (1995) ArticleTitleA model study on the infuence of a slowly activating potassium conductance on repetitive firing patterns of muscle spindle primary endings J theor Biol 173 56–67
A Prochazka (1996) Proprioceptive feedback and movement regulation LB Rowell JT Sheperd (Eds) Handbook of Physiology, Section 12 American Physiological Society New York 89–127
F Rieke D Warland R Ruyter Stevenink Particlede van W Bialek (1997) Spikes: exploring the neural code The MIT Press Cambridge
A Schaafsma E Otten DJ Willigen Particlevan (1991) ArticleTitleA muscle spindle model for primary afferent firing based on a simulation of intrafusal mechanical events J Neurophysiol 65 1297–1312 Occurrence Handle1:STN:280:By6A2c7lsF0%3D Occurrence Handle1831496
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423, 623–656
SP Strong R Koberle RR Ruyter Steveninck Particlede van W Bialek (1998) ArticleTitleEntropy and information in neural spike trains Phys Rev Lett 80 197–200 Occurrence Handle1:CAS:528:DyaK1cXislOjsQ%3D%3D
Subrahmanya P,Berger T,(1995) A sliding window Lempel-Ziv algorithm for differential layer encoding in progressive transmission In: Proceedings in 1995 IEEE internatinal symposium information theory Whistler, pp266
Tock Y (1999) Information transmition in the muscle spindle system.Master’s thesis,Technion,Haifa, Israel
Tock Y(2003) Information theoretic analysis of themuscle spindle system. PhD Thesis, Technion, Haifa, Israel
Y Tock M Ljubisavljevic J Thunberg U Windhorst GF Inbar H Johansson (2002) ArticleTitleInformation theoretic analysis of de-efferented single muscle spindles Biol Cybern 87 241–248 Occurrence Handle1:STN:280:DC%2BD38nivVehtQ%3D%3D Occurrence Handle12386740
DK Warland P Reinagel M Meister (1997) ArticleTitleDecoding visual information from a population of retinal ganglion cells J Neurophysiol 78 2336–2350 Occurrence Handle1:STN:280:DyaK1c%2FisVSlug%3D%3D Occurrence Handle9356386
AD Wyner J Ziv (1989) ArticleTitleSome asymptotic properties of the entropy of a stationary ergodic data source with applications to data compression IEEE Trans Inform Theory 35 1250–1258
AD Wyner J Ziv AJ Wyner (1998) ArticleTitle On the role of pattern matching in information theory IEEE Trans Inform Theory 44 2045–2056
J Ziv A Lempel (1977) ArticleTitleA universal algorithm for sequential data compression IEEE Trans Inform Theory 23 337–347
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tock, Y., Inbar, G., Steinberg, Y. et al. Estimation of muscle spindle information rate by pattern matching and the effect of gamma system activity on parallel spindles. Biol Cybern 92, 316–332 (2005). https://doi.org/10.1007/s00422-005-0552-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-005-0552-4