Experimental Brain Research

, Volume 112, Issue 3, pp 431–441 | Cite as

Neuronal assembly dynamics in the rat auditory cortex during reorganization induced by intracortical microstimulation

  • Pedro E. Maldonado
  • George L. Gerstein
Research Article


Single neurons, acting alone, cannot account for the complex and rapid computations that are routinely accomplished by the behaving nervous system. Recent studies with separable multineuron recordings are showing that neuronal assemblies can indeed be detected and that their organization is very dynamic, depending on variables such as time, physical stimulus, and context. Here we explore both single-neuron and assembly properties in the rat's auditory cortex. Acoustic stimuli are used as a normal, physiological input, and weak electrical intracortical microstimulation (ICMS) as a perturbation that forces a rapid cortical reorganization. In this setting, various aspects of neuronal interactions are changed by the ICMS. We found that cortical neurons exhibited highly synchronous oscillatory firing patterns that were enhanced by ICMS. Cross-correlation studies between two spike trains showed that statistically significant correlations depended on the anatomical distance between the two neurons. ICMS changed the strength and the local number of such correlations. Joint petristimulus analysis and gravity analysis showed that the correlation between neuronal activities varied dynamically at several time scales. We have identified neuronal assemblies in two ways, defined through similarity of receptive field properties and defined through correlated firing. Close anatomical spacing between neurons was conducive to, but not sufficient for membership in, the same assembly with either definition. ICMS changed cortical organization by altering assembly membership. Our data show that neuronal assemblies in the rat auditory cortex can be established transiently in time and that their membership is dynamic.

Key words

Plasticity Auditory cortex Neuronal assemblies Microstimulation Cortical maps Rat 


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  1. Aertsen AM, Gerstein GL, Habib MK, Palm G (1989) Dynamics of neuronal firing correlation: modulation of “effective connectivity”. J Neurophysiol 61:900–917Google Scholar
  2. Ahissar E, Vaadia E (1990) Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. Proc Natl Acad Sci USA 87:8135–8139Google Scholar
  3. Altman JA, Bekhterev NH, Kotelenko LM, Kudriavtseva IN (1980) Afterdischarges of cat medial geniculate body neurons. Fiziol Zh SSSR 66(1):80–8Google Scholar
  4. Ballard DH, Hinton GE, Sejnowski TJ (1983) Parallel visual computation. Nature 306:21–26Google Scholar
  5. Bedenbaugh P (1993) Plasticity in the rat somatosensory cortex induced by local microstimulation and theoretical investigations of information flow through neurons. PhD dissertation, Department of Bioengineering, University of PennsylvaniaGoogle Scholar
  6. Boch R (1986) Behavioral modulation of neuronal activity in monkey striate cortex: excitation in the absence of active central fixation. Exp Brain Res 64:610–614Google Scholar
  7. Deppisch J, Pawelzik K, Geisel T (1994) Uncovering the synchronization dynamics from correlated neuronal activity quantifies assembly formation. Biol Cybern 71(5):387–99Google Scholar
  8. Eckhorn R, Frien A, Bauer R, Woelbern T, Kehr H (1993) High frequency (60–90 Hz) oscillations in primary visual cortex of awake monkeys. Neuroreport 4:243–246Google Scholar
  9. Eggermont J (1992) Stimulus induced and spontaneous rhythmic firing of single units in cat primary visual cortex. Hear Res 61:1–11Google Scholar
  10. Engel AK, Kreiter AK, Koenig P, Singer W (1991) Interhemispheric synchronization of oscillatory neuronal responses in car visual cortex. Science 252:1177–1179Google Scholar
  11. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processes in the primary cerebral cortex. Cereb Cortex 1(1):1–47PubMedGoogle Scholar
  12. Gerstein GL, Aertsen AM (1985) Representation of cooperative firing activity among simultaneously recorded neurons. J Neurophysiol 54:1513–1528Google Scholar
  13. Gerstein GL, Perkel DH, Dayhoff JE (1985) Cooperative firing activity in simultaneously recorded populations of neurons: detection and measurements. J Neurophysiol 5:881–889Google Scholar
  14. Gerstein GL, Bedenbaugh P, Aertsen AM (1989) Neuronal assemblies. IEEE Trans Biomed Engl 36(1):4–14Google Scholar
  15. Glaser EM, Ruchkin DS (1976) Principles of neurobiological signal analysis. Academic, New YorkGoogle Scholar
  16. Gray C, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci 86:1698–1702Google Scholar
  17. Gray C, Koenig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337Google Scholar
  18. Gray C, Engel AK, Koenig P, Singer W (1992) Synchronization of oscillatory neuronal responses in cat striate cortex. Temporal properties. Vis Neurosci 8:337–347Google Scholar
  19. Gross CG, Rocha-Miranda CE, Bender BE (1972) Visual properties of neurons in the inferotemporal cortex of the macaque. J Neurophysiol 35:96–112Google Scholar
  20. Hata Y, Tsumoto T, Sato H, Hagihara K, Tamura T (1993) Development of local horizontal interactions in the cat visual cortex studied by cross-correlation analysis. J Neurophysiol 69:40–56Google Scholar
  21. Lettvin JY, Maturana HR, McCulloch WS, Pitts WH (1959) What the frog's eye tells the frog's brain. Proc IRE 47(11):1940–1951Google Scholar
  22. Lindsey BG, Segers LS, Morris KF, Hernandez KM, Saporta S, Shannon R (1994) Distributed actions and dynamic associations in respiratory-related neuronal assemblies of the ventrolateral medulla and brain stem midline: evidence from spike train analysis. J Neurophysiol 72(4):1830–51Google Scholar
  23. Llinas R, Grace AA, Yarom Y (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc Natl Acad Sci USA 88:897–901Google Scholar
  24. Lowel S, Singer W (1992) Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255:209–212Google Scholar
  25. Maldonado PE, Gerstein GL (1996) Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study. Exp Brain Res 112:420–430Google Scholar
  26. Malsburg C von der, Singer W (1988) Principles of cortical network organization. In: Radik P, Singer W (eds) Neurobiology of neocortex. Wiley and Sons, New York, pp 69–99Google Scholar
  27. McCormick DA, Gray CM (1995) Physiologically identified cell groups have distinct receptive field and morphological properties in cat striate cortex. Soc Neurosci Abstr 21 (2): 1506Google Scholar
  28. Palm G, Aertsen AM, Gerstein GL (1988) On the significance of correlations among neuronal spike trains. Biol Cybern 59:1–11Google Scholar
  29. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stocastic point processes. II. Simultaneous spike trains. Biophys J 7(4):419–440Google Scholar
  30. Sheperd G (1990) The synaptic organization of the brain. Oxford University Press, OxfordGoogle Scholar
  31. Silva LR, Amitai Y, Connors BW (1991) Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251:432–435Google Scholar
  32. Singer W (1991) The formation of cooperative cell assemblies in the visual cortex. In: Kruger J (ed) Neuronal cooperativity. Springer, Berlin Heidelberg New York, pp 165–183Google Scholar
  33. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation analysis. Annu Rev Neurosci 18:555–586Google Scholar
  34. Toyama K, Kimura M, Tanaka K (1981) Cross-correlation analysis of interneuronal connectivity in cat visual cortex. J Neurophysiol 46:191–201Google Scholar
  35. Tso D (1991) Connectivity and functional organization in the mammalian visual cortex. In: Kruger J (ed) Neuronal cooperativity. Springer, Berlin Heidelberg New York, pp 249–279Google Scholar
  36. Vaadia E, Ahissar E, Bergman H, Lavner Y (1991) Correlated activity of neurons: a neural code for higher brain functions? In: Kruger J (ed) Neuronal cooperativity. Springer, Berlin Heidelberg New York, pp 249–279Google Scholar
  37. White EL (1989) Cortical circuits. Birkhauser, BostonGoogle Scholar
  38. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373 (6515):612–615CrossRefGoogle Scholar
  39. Young MP, Yamane S (1992) Sparse population coding of faces in the inferotemporal cortex. Science 256 (5061):1327–1331Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Pedro E. Maldonado
    • 1
  • George L. Gerstein
    • 1
  1. 1.Department of NeuroscienceSchool of Medicine, University of PennsylvaniaPhiladelphiaUSA

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