Abstract
Using a rat model to study the cellular effects of repetitive transcranial magnetic stimulation (rTMS) with regard to changes in cortical excitability, we previously described opposite effects of continuous and intermittent theta-burst stimulation (cTBS, iTBS) on the expression of the calcium-binding proteins (CaBP) parvalbumin (PV), calbindin (CB) and calretinin (CR) in Dark Agouti rats (DA). While iTBS significantly reduced the number of cortical PV+ cells but did not affect the CB+ cells, cTBS resulted in a decrease in CB+ cells with no effects on PV+ cells. We concluded that activity of these classes of cortical interneurons is differently modulated by iTBS and cTBS. When testing two further rat strains, Sprague–Dawley (SD) and Long Evans (LE), we obtained deviating results. In SD, iTBS reduced PV and CB expression, while cTBS only reduced PV expression. In contrast, reanalysed DA showed reduced CB expression after cTBS and reduced PV expression after iTBS, while LE shows an intermediate reaction. CR expression was unaffected in any case. Interestingly, we found significantly different basal expression patterns of the CaBPs for the strains, with DA and LE showing much higher numbers of PV+, CB+ and CR+ cells than SD, and with particularly higher number of CB+ and CR+ cells in DA compared to the other two strains. These findings demonstrate that inhibitory systems may be either differently developed in rats belonging to diverse strains or show different basal levels of activity and CaBP expression and may therefore be differently sensitive to the rTMS protocols.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126–130
Abrahám H, Tóth Z, Bari F, Domoki F, Seress L (2005) Novel calretinin and reelin expressing neuronal population includes Cajal-Retzius-type cells in the neocortex of adult pigs. Neuroscience 136:217–230
Ascoli GA, The Petilla Interneuron Nomenclature Group (PING) (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568
Barinka F, Druga R (2010) Calretinin expression in the mammalian neocortex: a review. Physiol Res 59:665–677
Benali A, Trippe J, Weiler E, Mix A, Petrasch-Parwez E, Girzalsky W, Eysel UT, Erdmann R, Funke K (2011) Theta-burst transcranial magnetic stimulation alters cortical inhibition. J Neurosci 31:1193–1203
Caputi A, Rozov A, Blatow M, Monyer H (2009) Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. Cereb Cortex 19:1345–1359
Cárdenas-Morales L, Volz LJ, Michely J, Rehme AK, Pool EM, Nettekoven C, Eickhoff SB, Fink GR, Grefkes C (2013) Network connectivity and individual responses to brain stimulation in the human motor system. Cereb Cortex doi:10.1093/cercor/bht023
Chaudhury S, Nag TC, Wadhwa S (2008) Calbindin D-28 K and parvalbumin expression in embryonic chick hippocampus is enhanced by prenatal auditory stimulation. Brain Res 1191:96–106
Di Lazzaro V, Profice P, Ranieri F, Capone F, Dileone M, Oliviero A, Pilato F (2012) I-wave origin and modulation. Brain Stimul 5:512–525
Freund TF (2003) Interneuron Diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489–495
Funke K, Benali A (2011) Modulation of cortical inhibition by rTMS—findings obtained from animal models. J Physiol Lond 589:4423–4435
Gonchar Y, Burkhalter A (1999) Connectivity of GABAergic calretinin-immunoreactive neurons in rat primary visual cortex. Cereb Cortex 9:683–696
Gonchar Y, Burkhalter A (2003) Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J Neurosci 23:10904–10912
Gonchar Y, Wang Q, Burkhalter A (2008) Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. doi10.3389/neuro.05.003.2007
Hamada M, Murase N, Hasan A, Balaratnam M, Rothwel JC (2012) The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex 23:1593–1605
Hoppenrath K, Funke K (2013) Time-course of changes in neuronal activity markers following iTBS-TMS of the rat neocortex. Neurosci Lett 536:19–23
Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206
Kawaguchi Y, Kubota Y (1996) Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16:2701–2715
Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793–807
Mechan AO, Moran PM, Elliott JM, Young AMJ, Joseph MH, Green AR (2002) A comparison between Dark Agouti and Sprague-Dawley rats in their behaviour on the elevated plus-maze, open-field apparatus and activity meters, and their response to diazepam. Psychopharmacol 159:188–195
Melchitzky DS, Lewis DA (2003) Pyramidal neuron local axon terminals in monkey prefrontal cortex: differential targeting of subclasses of GABA neurons. Cereb Cortex 13:452–460
Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379:113–132
Michaluk J, Antkiewicz-Michaluk L, Vetulani J (2001) Conditions of application of repeated transcranial magnetic stimulation to rats may mask the effects of the treatment. Pol J Pharmacol 53:685e7
Patz S, Grabert J, Gorba T, Wirth MJ, Wahle P (2004) Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an early period of postnatal development. Cereb Cortex 14:342–351
Pell GS, Roth Y, Zangen A (2011) Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol 93:59–98
Ridding MC, Ziemann U (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol Lond 588:2291–2304
Rotenberg A, Muller PA, Vahabzadeh-Hagh AM, Navarro X, López-Vales R, Pascual-Leone A, Jensen F (2010) Lateralization of forelimb motor evoked potentials by transcranial magnetic stimulation in rats. Clin Neurophysiol 121:104–108
Rushton WA (1927) The effect upon the threshold for nervous excitation of the length of nerve exposed, and the angle between current and nerve. J Physiol 63:357–377
Schwaller B (2009) The continuing disappearance of ‘pure’ Ca2+ buffers. Cell Mol Life Sci 66:275–300
Tepper JM, Tecuapetla F, Koós T, Ibáñez-Sandoval O (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4:150
Trippe J, Mix A, Aydin-Abidin S, Funke K, Benali A (2009) Theta burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex. Exp Brain Res 199:411–421
Volz LJ, Benali A, Mix A, Neubacher U, Funke K (2013) Dose-dependence of changes in cortical protein expression induced with repeated transcranial magnetic theta-burst stimulation in the rat. Brain Stimul 6:598–606
Acknowledgments
The authors are grateful to Dimitrula Winkler, Ute Neubacher and Tanja Ishorst for support in immunohistochemical techniques and handling of rats during rTMS procedures. This study has been partly supported by a fund of the Deutsche Forschungsgemeinschaft (DFG) to K. Funke (SFB 874, TP A4).
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mix, A., Benali, A. & Funke, K. Strain differences in the effect of rTMS on cortical expression of calcium-binding proteins in rats. Exp Brain Res 232, 435–442 (2014). https://doi.org/10.1007/s00221-013-3751-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-013-3751-6