Abstract
Objective
The well-established planar multi-electrode array recording technique was used to investigate neural circuits and temporal plasticity in the hindlimb representation of the rat primary somatosensory cortex (S1 area).
Methods
Freshly dissociated acute brain slices of rats were subject to constant perfusion with oxygenated artificial cerebrospinal fluid (95% O2 and 5% CO2), and were mounted on a Med64 probe (64 electrodes, 8×8 array) for simultaneous multi-site electrophysiological recordings. Current sources and sinks across all the 64 electrodes were transformed into two-dimensional current source density images by bilinear interpolation at each point of the 64 electrodes.
Results
The local intracortical connection, which is involved in mediation of downward information flow across layers II–VI, was identified by electrical stimulation (ES) at layers II–III. The thalamocortical connection, which is mainly involved in mediation of upward information flow across layers II–IV, was also characterized by ES at layer IV. The thalamocortical afferent projections were likely to make more synaptic contacts with S1 neurons than the intracortical connections did. Moreover, the S1 area was shown to be more easily activated and more intensively innervated by the thalamocortical afferent projections than by the intracortical connections. Finally, bursting conditioning stimulus (CS) applied within layer IV of the S1 area could successfully induce long-term potentiation (LTP) in 5 of the 6 slices (83.3%), while the same CS application at layers II–III induced no LTP in any of the 6 tested slices.
Conclusion
The rat hindlimb representation of S1 area is likely to have at least 2 patterns of neural circuits on brain slices: one is the intracortical circuit (ICC) formed by interlaminar connections from layers II–III, and the other is the thalamocortical circuit (TCC) mediated by afferent connections from layer IV. Besides, ICC of the S1 area is spatially limited, with less plasticity, while TCC is spatially extensive and exhibits a better plasticity in response to somatosensory afferent stimulation. The present data provide a useful experimental model for further studying microcircuit properties in S1 cortex at the network level in vitro.
Keywords: planar multi-electrode array, two-dimensional current source density imaging, primary somatosensory cortex, neural circuits, long-term potentiation
摘要
目的
运用平面微电极阵列记录技术探讨大鼠初级躯体感觉皮层(primary somatosensory cortex, S1 area)后肢代表区的神经回路和时间可塑性。
方法
将急性分离的大鼠脑片置于MED-64 系统的电极平皿中, 持续灌流通入 95% O2 和5% CO2 混合气的人工脑脊液, 随后进行多电极同时同步记录。 利用双线性内插法计算出64个点的电流源与电流井, 并将其转换为二维电流源密度分布图。
结果
刺激S1 后肢代表区脑片的II–III层, 可鉴定出局部皮层内的连接回路, 而刺激IV 层(丘脑传入的主要终末端)则鉴定出丘脑皮层间的连接回路。 首先, 丘脑皮层投射的激活可以诱发更多的有效场电位, 并且与S1 区更多的神经元建立突触联系。 与之相比, 皮层内回路的激活引起的电反应活动范围则较小。 其次, 刺激IV 层在每一刺激强度下诱发的场电位幅度远远大于刺激II–III的场电位幅度, 即S1 区更容易被丘脑皮层连接回路的投射纤维所激活。 最后, 在S1 区IV 层给予强直刺激可以记录到长达两个小时的局部场电位幅度的增加, 长时程增强(long-term potentiation, LTP)的诱出率约为83.3% (5/6 例)。 相反, 在II–III层, 同样的强直刺激并未能明显诱导LTP的发生。
结论
大鼠S1区的后肢代表区似乎存在两种不同类型的神经回路, 一种是由层间联系介导的皮层内回路, 另一种则是由丘脑皮层传入介导的丘脑皮层连接回路。 皮层内回路在空间上联系较局限且可塑性不强, 而丘脑皮层回路的空间连接范围则相对较广, 对躯体感觉信息的传入也显示出很强的可塑性。 本结果为进一步在体外神经网络水平研究S1 区的神经回路特性提供了很好的实验模型。
关键词: 平面微电极阵列记录技术, 二维电流源密度分析, 初级躯体感觉皮层, 神经回路, 长时程增强
References
- [1].Knierim J. Information processing in neural networks. In: Byrne J., Roberts J., editors. From molecules to networks. Amsterdam: Elsevier Academic Press; 2009. pp. 513–537. [Google Scholar]
- [2].Byrne J., LaBar K., LeDoux J., Schafe G., Sweatt J., Thompson R. Learning and memory: Basic mechanisms. In: Byrne J., Roberts J., editors. From molecules to networks. Amsterdam: Elsevier Academic Press; 2009. pp. 539–608. [Google Scholar]
- [3].Mountcastle V. Perceptual neuroscience: The cerebral cortex. Cambridge: Harvard University Press; 1998. p. 486. [Google Scholar]
- [4].Jaw F.S., Kao Y.C., Chen C.P., Liao W.L. Cerebral columnar organization of the first nociceptive component induced by CO2 laser on the tail of the rat. Neuroscience. 2009;158(2):945–950. doi: 10.1016/j.neuroscience.2008.09.046. [DOI] [PubMed] [Google Scholar]
- [5].Salin P.A., Prince D.A. Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol. 1996;75(4):1573–1588. doi: 10.1152/jn.1996.75.4.1573. [DOI] [PubMed] [Google Scholar]
- [6].Zhang Z.W., Deschenes M. Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study. J Neurosci. 1997;17(16):6365–6379. doi: 10.1523/JNEUROSCI.17-16-06365.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [7].Bodor A.L., Katona I., Nyiri G., Mackie K., Ledent C., Hajos N., et al. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci. 2005;25(29):6845–6856. doi: 10.1523/JNEUROSCI.0442-05.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [8].Cauli B., Audinat E., Lambolez B., Angulo M.C., Ropert N., Tsuzuki K., et al. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci. 1997;17(10):3894–3906. doi: 10.1523/JNEUROSCI.17-10-03894.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [9].Lamour Y., Guilbaud G., Willer J.C. Rat somatosensory (SmI) cortex: II. Laminar and columnar organization of noxious and non-noxious inputs. Exp Brain Res. 1983;49(1):46–54. doi: 10.1007/BF00235540. [DOI] [PubMed] [Google Scholar]
- [10].Lamour Y., Willer J.C., Guilbaud G. Rat somatosensory (SmI) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation. Exp Brain Res. 1983;49(1):35–45. doi: 10.1007/BF00235539. [DOI] [PubMed] [Google Scholar]
- [11].Taketani M., Baudry M. Advances in network electrophysiology: Using multi-electrode arrays. Singapore: Springer; 2006. p. 478. [Google Scholar]
- [12].Colgin L.L., Moser E.I. Neuroscience: rewinding the memory record. Nature. 2006;440(7084):615–617. doi: 10.1038/440615a. [DOI] [PubMed] [Google Scholar]
- [13].Duport S., Millerin C., Muller D., Correges P. A metallic multisite recording system designed for continuous long-term monitoring of electrophysiological activity in slice cultures. Biosens Bioelectron. 1999;14(4):369–376. doi: 10.1016/S0956-5663(99)00015-9. [DOI] [PubMed] [Google Scholar]
- [14].Hofmann F., Bading H. Long term recordings with microelectrode arrays: studies of transcription-dependent neuronal plasticity and axonal regeneration. J Physiol (Paris) 2006;99(2–3):125–132. doi: 10.1016/j.jphysparis.2005.12.005. [DOI] [PubMed] [Google Scholar]
- [15].Morin F.O., Takamura Y., Tamiya E. Investigating neuronal activity with planar microelectrode arrays: achievements and new perspectives. J Biosci Bioeng. 2005;100(2):131–143. doi: 10.1263/jbb.100.131. [DOI] [PubMed] [Google Scholar]
- [16].Steidl E.M., Neveu E., Bertrand D., Buisson B. The adult rat hippocampal slice revisited with multi-electrode arrays. Brain Res. 2006;1096(1):70–84. doi: 10.1016/j.brainres.2006.04.034. [DOI] [PubMed] [Google Scholar]
- [17].van Bergen A., Papanikolaou T., Schuker A., Moller A., Schlosshauer B. Long-term stimulation of mouse hippocampal slice culture on microelectrode array. Brain Res Protoc. 2003;11(2):123–133. doi: 10.1016/S1385-299X(03)00024-2. [DOI] [PubMed] [Google Scholar]
- [18].Shimono K., Brucher F., Granger R., Lynch G., Taketani M. Origins and distribution of cholinergically induced beta rhythms in hippocampal slices. J Neurosci. 2000;20(22):8462–8473. doi: 10.1523/JNEUROSCI.20-22-08462.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [19].Shimono K., Kubota D., Brucher F., Taketani M., Lynch G. Asymmetrical distribution of the Schaffer projections within the apical dendrites of hippocampal field CA1. Brain Res. 2002;950(1–2):279–287. doi: 10.1016/S0006-8993(02)03052-4. [DOI] [PubMed] [Google Scholar]
- [20].Zhao X.Y., Liu M.G., Yuan D.L., Wang Y., He Y., Wang D.D., et al. Nociception-induced spatial and temporal plasticity of synaptic connection and function in the hippocampal formation of rats: a multi-electrode array recording. Mol Pain. 2009;5:55. doi: 10.1186/1744-8069-5-55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [21].Krause M., Jia Y. Serotonergic modulation of carbachol-induced rhythmic activity in hippocampal slices. Neuropharmacology. 2005;48(3):381–390. doi: 10.1016/j.neuropharm.2004.10.011. [DOI] [PubMed] [Google Scholar]
- [22].Oka H., Shimono K., Ogawa R., Sugihara H., Taketani M. A new planar multielectrode array for extracellular recording: application to hippocampal acute slice. J Neurosci Methods. 1999;93(1):61–67. doi: 10.1016/S0165-0270(99)00113-2. [DOI] [PubMed] [Google Scholar]
- [23].He Y., Liu M.G., Gong K.R., Chen J. Differential effects of long and short train theta burst stimulation on LTP induction in rat anterior cingulate cortex slices: multi-electrode array recordings. Neurosci Bull. 2009;25(5):309–318. doi: 10.1007/s12264-009-0831-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [24].Agmon A., Connors B.W. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience. 1991;41(2–3):365–379. doi: 10.1016/0306-4522(91)90333-J. [DOI] [PubMed] [Google Scholar]
- [25].Kotter R., Staiger J.F., Zilles K., Luhmann H.J. Analysing functional connectivity in brain slices by a combination of infrared video microscopy, flash photolysis of caged compounds and scanning methods. Neuroscience. 1998;86(1):265–277. doi: 10.1016/S0306-4522(98)00010-4. [DOI] [PubMed] [Google Scholar]
- [26].Bakker R., Schubert D., Levels K., Bezgin G., Bojak I., Kotter R. Classification of cortical microcircuits based on micro-electrodearray data from slices of rat barrel cortex. Neural Netw. 2009;22(8):1159–1168. doi: 10.1016/j.neunet.2009.07.014. [DOI] [PubMed] [Google Scholar]
- [27].Staiger J.F., Kotter R., Zilles K., Luhmann H.J. Laminar characteristics of functional connectivity in rat barrel cortex revealed by stimulation with caged-glutamate. Neurosci Res. 2000;37(1):49–58. doi: 10.1016/S0168-0102(00)00094-8. [DOI] [PubMed] [Google Scholar]
- [28].Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 5th ed. San Diego: Elsevier Academic Press; 2005. p. 367. [Google Scholar]
- [29].Burkhalter A. Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. J Comp Neurol. 1989;279(2):171–186. doi: 10.1002/cne.902790202. [DOI] [PubMed] [Google Scholar]
- [30].Callaway E.M., Wiser A.K. Contributions of individual layer 2–5 spiny neurons to local circuits in macaque primary visual cortex. Vis Neurosci. 1996;13(5):907–922. doi: 10.1017/S0952523800009159. [DOI] [PubMed] [Google Scholar]
- [31].Gilbert C.D., Wiesel T.N. Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature. 1979;280(5718):120–125. doi: 10.1038/280120a0. [DOI] [PubMed] [Google Scholar]
- [32].Hubel D.H., Wiesel T.N. Receptive fields and functional architecture of monkey striate cortex. J Physiol. 1968;195(1):215–243. doi: 10.1113/jphysiol.1968.sp008455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [33].Petersen C.C., Sakmann B. The excitatory neuronal network of rat layer 4 barrel cortex. J Neurosci. 2000;20(20):7579–7586. doi: 10.1523/JNEUROSCI.20-20-07579.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [34].Chang Y., Yan L.H., Zhang F.K., Gong K.R., Liu M.G., Xiao Y., et al. Spatiotemporal characteristics of pain-associated neuronal activities in primary somatosensory cortex induced by peripheral persistent nociception. Neurosci Lett. 2008;448(1):134–138. doi: 10.1016/j.neulet.2008.08.090. [DOI] [PubMed] [Google Scholar]
- [35].Feldmeyer D., Sakmann B. Synaptic efficacy and reliability of excitatory connections between the principal neurones of the input (layer 4) and output layer (layer 5) of the neocortex. J Physiol. 2000;525(Pt1):31–39. doi: 10.1111/j.1469-7793.2000.00031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [36].Alloway K.D., Johnson M.J., Wallace M.B. Thalamocortical interactions in the somatosensory system: interpretations of latency and cross-correlation analyses. J Neurophysiol. 1993;70(3):892–908. doi: 10.1152/jn.1993.70.3.892. [DOI] [PubMed] [Google Scholar]
- [37].Gottlieb J.P., Keller A. Intrinsic circuitry and physiological properties of pyramidal neurons in rat barrel cortex. Exp Brain Res. 1997;115(1):47–60. doi: 10.1007/PL00005684. [DOI] [PubMed] [Google Scholar]
- [38].Heusler P., Cebulla B., Boehmer G., Dinse H.R. A repetitive intracortical microstimulation pattern induces long-lasting synaptic depression in brain slices of the rat primary somatosensory cortex. Exp Brain Res. 2000;135(3):300–310. doi: 10.1007/s002210000530. [DOI] [PubMed] [Google Scholar]
- [39].Roman F.S., Truchet B., Marchetti E., Chaillan F.A., Soumireu-Mourat B. Correlations between electrophysiological observations of synaptic plasticity modifications and behavioral performance in mammals. Prog Neurobiol. 1999;58(1):61–87. doi: 10.1016/S0301-0082(98)00076-8. [DOI] [PubMed] [Google Scholar]
- [40].Bear M.F., Kirkwood A. Neocortical long-term potentiation. Curr Opin Neurobiol. 1993;3(2):197–202. doi: 10.1016/0959-4388(93)90210-P. [DOI] [PubMed] [Google Scholar]
- [41].Castro-Alamancos M.A., Donoghue J.P., Connors B.W. Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J Neurosci. 1995;15(7Pt2):5324–5333. doi: 10.1523/JNEUROSCI.15-07-05324.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
