Experimental Brain Research

, Volume 107, Issue 2, pp 241–253 | Cite as

Synaptic plasticity induced in single neurones of the primary somatosensory cortex in vivo

  • Peter M. B. Cahusac
Research Article


Experiments carried out in urethane-anaesthetized rats in which single neurones were recorded extracellularly from primary somatosensory (SI) cortex employed a procedure in which one of two vibrissal inputswas temporally paired with iontophoretic applications of glutamate. Following the pairing procedure, 31% of 49 neurones studied displayed some form of synaptic plasticity, in that responses to one or both vibrissal stimuli were altered. Homosynaptic potentiation occurred in 4 neurones, and these were recorded in layers II/III only. Homosynaptic depression occurred in 6 neurones and were mainly recorded in layer IV. Heterosynaptic depression was observed in 3 neurones. Non-selective depression was observed in 2 neurones. The duration of the induced plastic changes typically exceeded 15 min, and often lasted as long as stable recordings continued. The results from experiments in which repeated glutamate applications were given alone (without synaptic input) confirmed that the non-selective changes were due to repeated glutamate applications and not the temporal pairing with synaptic responses per se. Dual recordings confirmed that plasticity was restricted to the neurone at which pairings were made, and (at the other neurone) that synaptic responses remained stable over the course of study. In some neurones homosynaptic potentiation and depression were shown to occur to the early response component (<10 ms), suggesting that direct thalamocortical synapses are modifiable.

Key words

Homosynaptic Heterosynaptic Long-term potentiation Long-term depression Barrel cortex Iontophoresis Glutamate Rat 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Armstrong-James M, Fox K (1987) Spatiotemporal convergence and divergence in the rat S1 “barrel” cortex. J Comp Neurol 263:265–281Google Scholar
  2. Armstrong-James M, Millar JM (1979) Carbon fibre microelectrodes. J Neurosci Methods 1:279–287Google Scholar
  3. Armstrong-James M, Millar JM (1980) A method for etching the tips of carbon fibre microelectrodes. J Neurosci Methods 2:431–432Google Scholar
  4. Armstrong-James M, Welker E (1993) Different roles for NMDA and non-NMDA receptors in fast and slow sensory transmission by rat SI barrel cortex neurones in vivo (abstract). J Physiol(Lond) 467:91PGoogle Scholar
  5. Armstrong-James M, Callahan CA, Friedman MA (1991) Thalamo-cortical processing of vibrissal information in the rat. I. Intracortical origins of surround but not centre-receptive fields of layer IV neurones in the rat S1 barrel field cortex. J Comp Neurol 303:193–210Google Scholar
  6. Armstrong-James M, Welker E, Callahan CA (1993) The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat S1 barrel cortex. J Neurosci 13:2149–2160Google Scholar
  7. Artola A, Singer W (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16:480–487Google Scholar
  8. Artola A, Braöcher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and longterm potentiation in slices of rat visual cortex. Nature 347:69–72Google Scholar
  9. Baranyi A, Szente MB, Woody CD (1991) Properties of associative long-lasting potentiation induced by cellular conditioning in the motor cortex of conscious cats. Neuroscience 42:321–334Google Scholar
  10. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32–48Google Scholar
  11. Bindman LJ, Murphy KPSJ, Pockett S (1988) Postsynaptic control of the induction of long-term changes in efficacy of transmission at neocortical synapses in slices of rat brain. J Neurophysiol 60:1053–1065Google Scholar
  12. Bortolotto ZA, Bashir ZI, Davies CH, Collingridge GL (1994) A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 368:740–743Google Scholar
  13. Cahusac PMB (1993) Synaptic plasticity induced by pairing vibrissal-evoked neuronal responses with iontophoretic glutamate in primary somatosensory cortex of the anaesthetized rat (abstract). J Physiol (Lond) 467:92PGoogle Scholar
  14. Cahusac PMB (1994) Cortical layer-specific effects of the metabotropic glutamate receptor agonist 1S,3R-ACPD in rat primary somatosensory cortex in vivo. Eur J Neurosci 6:1505–1511Google Scholar
  15. Cahusac PMB, Rolls ET, Marriott FHC (1991) Potentiation of neuronal responses to natural visual input paired with postsynaptic activation in the hippocampus of the awake monkey. Neurosci Lett 124:39–43Google Scholar
  16. Collingridge GL, Singer W (1990) Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 11:290–296Google Scholar
  17. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99–104Google Scholar
  18. Conti F, Rustioni A, Petrusz P (1987) Co-localization of glutamate and aspartate immunoreactivity in neurons of the rat somatic sensory cortex. In: Excitatory amino acid transmission. Hicks TP, Lodge D, McLennan H (eds) Liss, New York, pp 169–172Google Scholar
  19. Cooper LN, Liberman F, Oja E (1979) A theory for the acquisition and loss of neuron specificity in visual cortex. Biol Cybern 33:9–28Google Scholar
  20. Delacour J, Houcine O, Talbi B (1987) “Learned” changes in the responses of the rat barrel field neurons. Neuroscience 23:63–71Google Scholar
  21. Diamond ME, Armstrong-James M, Ebner FF (1993) Experiencedependent plasticity in adult rat barrel cortex. Proc Natl Acad Sci USA 90:2082–2086Google Scholar
  22. Frégnac Y, Shulz D, Thorpe S, Bienenstock E (1992) Cellular analogs of visual cortical epigenesis. I. Plasticity of orientation selectivity. J Neurosci 12:1280–1300Google Scholar
  23. Greuel JM, Luhmann HJ, Singer W (1988) Pharmacological induction of use-dependent receptive field modifications in the visual cortex. Science 242:74–77Google Scholar
  24. Hebb DO (1949) The organization of behavior. Wiley & Sons, New YorkGoogle Scholar
  25. Hirsch JC, Crepel F (1990) Use-dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. J Physiol (Lond) 427:31–49Google Scholar
  26. Iriki A, Pavlides C, Keller A, Asanuma H (1991) Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents. J Neurophysiol 65:1435–1441Google Scholar
  27. Ito M (1985) Processing of vibrissa sensory information within the rat neocortex. J Neurophysiol 54:479–490Google Scholar
  28. Kaas JH, Merzenich MM, Killackey HP (1983) The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Annu Rev Neurosci 6:325–356Google Scholar
  29. Lee SM, Ebner FF (1992) Induction of high-frequency activity in the somatosensory thalamus of rats in vivo results in long-term potentiation of responses in SI cortex. Exp Brain Res 90:253–261Google Scholar
  30. Malinow R, Miller JP (1986) Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320:529–530Google Scholar
  31. Pockett S, Brookes NH, Bindman LJ (1990) Long-term depression at synapses in slices of rat hippocampus can be induced by bursts of postsynaptic activity. Exp Brain Res 80:196–200Google Scholar
  32. Schoepp DD, Conn PJ (1993) Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol Sci 14:13–20Google Scholar
  33. Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41:798–820Google Scholar
  34. Simons DJ, Land PW (1987) Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326:694–697Google Scholar
  35. Simons DJ, Carvell GE, Land PW (1989) The vibrissa/barrel cortex as a model of sensory information processing. In: Lund JS (ed) Sensory processing in the mammalian brain. Oxford University Press, New York, pp 67–83Google Scholar
  36. Stent GS (1973) A physiological mechanism for Hebb's postulate of learning. Proc Natl Acad Sci USA 70:997–1001Google Scholar
  37. Tremblay N, Warren RA, Dykes RW (1990) Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. J Neurophysiol 64:1212–1222Google Scholar
  38. Tsumoto T (1992) Long-term potentiation and long-term depression in the neocortex. Prog Neurobiol 39:209–228Google Scholar
  39. Watkins JC, Krogsgaard-Larsen P, Honoré T (1990) Structure-activity relationships in the development of excitatory amino acid receptor agonists and competitive antagonists. Trends Pharmacol 11:25–33Google Scholar
  40. Wiesel TN, Hubel DH (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 28:1029–1040Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Peter M. B. Cahusac
    • 1
  1. 1.Department of PsychologyUniversity of StirlingStirlingScotland, UK

Personalised recommendations