[en] The long-range coupling within prefrontal-hippocampal networks that account for cognitive performance emerges early in life. The discontinuous hippocampal theta bursts have been proposed to drive the generation of neonatal prefrontal oscillations, yet the cellular substrate of these early interactions is still unresolved. Here, we selectively target optogenetic manipulation of glutamatergic projection neurons in the CA1 area of either dorsal or intermediate/ventral hippocampus at neonatal age to elucidate their contribution to the emergence of prefrontal oscillatory entrainment. We show that despite stronger theta and ripples power in dorsal hippocampus, the prefrontal cortex is mainly coupled with intermediate/ventral hippocampus by phase-locking of neuronal firing via dense direct axonal projections. Theta band-confined activation by light of pyramidal neurons in intermediate/ventral but not dorsal CA1 that were transfected by in utero electroporation with high-efficiency channelrhodopsin boosts prefrontal oscillations. Our data causally elucidate the cellular origin of the long-range coupling in the developing brain.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Ahlbeck, Joachim ; Developmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Song, Lingzhen; Developmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Chini, Mattia ; Developmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Bitzenhofer, Sebastian H; Developmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Hanganu-Opatz, Ileana L ; Developmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Language :
English
Title :
Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse.
ERC - European Research Council DFG - Deutsche Forschungsgemeinschaft
Funding text :
We thank Nadine Faesel for the establishment of tracing technique, Antonio Candela for preliminary tracing data, Drs. L Cancedda and A Cwetsch for help with the in utero electroporation, Drs. S Wie-gert, T Oertner, and C Gee for help with the development of opsin constructs as well as A Mar-quardt, P Putthoff, A Dahlmann and I Ohmert for excellent technical assistance. ILH-O acknowledges support by the ERC (ERC Consolidator Grant 681577) and by the German Research Foundation (SFB 936 (B5) and SPP 1665 (Ha4466/12-1)). ILH-O is the member of the FENS Kavli Network of Excellence. In memoriam of Howard Eichenbaum
Adhikari A, Topiwala MA, Gordon JA. 2010. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65:257–269. DOI: https://doi.org/10.1016/j.neuron.2009.12. 002, PMID: 20152131
Amaral DG, Scharfman HE, Lavenex P. 2007. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Progress in Brain Research 163:3–22. DOI: https://doi.org/10.1016/S0079-6123 (07)63001-5, PMID: 17765709
Baccala LA, Sameshima K, Takahashi DY. 2007. Generalized Partial Directed Coherence. 15th International Conference on Digital Signal Processing 163–166.
Bast T, Wilson IA, Witter MP, Morris RG. 2009. From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biology 7:e1000089. DOI: https://doi.org/10.1371/journal.pbio. 1000089, PMID: 19385719
Baumgart J, Grebe N. 2015. C57BL/6-specific conditions for efficient in utero electroporation of the central nervous system. Journal of Neuroscience Methods 240:116–124. DOI: https://doi.org/10.1016/j.jneumeth.2014. 11.004, PMID: 25445056
Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. 1989. Giant synaptic potentials in immature rat CA3 hippocampal neurones. The Journal of Physiology 416:303–325. DOI: https://doi.org/10.1113/jphysiol.1989. sp017762, PMID: 2575165
Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI. 2010. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66:921–936. DOI: https://doi.org/10.1016/j.neuron.2010.05.013, PMID: 20620877
Berndt A, Schoenenberger P, Mattis J, Tye KM, Deisseroth K, Hegemann P, Oertner TG. 2011. High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. PNAS 108:7595–7600. DOI: https://doi.org/10.1073/pnas.1017210108, PMID: 21504945
Bitzenhofer SH, Hanganu-Opatz IL. 2014. Oscillatory coupling within neonatal prefrontal-hippocampal networks is independent of selective removal of GABAergic neurons in the hippocampus. Neuropharmacology 77:57–67. DOI: https://doi.org/10.1016/j.neuropharm.2013.09.007, PMID: 24056266
Bitzenhofer SH, Sieben K, Siebert KD, Spehr M, Hanganu-Opatz IL. 2015. Oscillatory activity in developing prefrontal networks results from theta-gamma-modulated synaptic inputs. Cell Reports 11:486–497. DOI: https://doi.org/10.1016/j.celrep.2015.03.031, PMID: 25865885
Bitzenhofer SH, Ahlbeck J, Hanganu-Opatz IL. 2017a. Methodological Approach for Optogenetic Manipulation of Neonatal Neuronal Networks. Frontiers in Cellular Neuroscience 11:239–252. DOI: https://doi.org/10.3389/fncel.2017.00239, PMID: 28848399
Borrell V, Yoshimura Y, Callaway EM. 2005. Targeted gene delivery to telencephalic inhibitory neurons by directional in utero electroporation. Journal of Neuroscience Methods 143:151–158. DOI: https://doi.org/10. 1016/j.jneumeth.2004.09.027, PMID: 15814147
Brincat SL, Miller EK. 2015. Frequency-specific hippocampal-prefrontal interactions during associative learning. Nature Neuroscience 18:576–581. DOI: https://doi.org/10.1038/nn.3954, PMID: 25706471
Brockmann MD, Pöschel B, Cichon N, Hanganu-Opatz IL. 2011. Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat. Neuron 71:332–347. DOI: https://doi.org/10.1016/j.neuron.2011.05.041, PMID: 21791291
Buhl DL, Buzsáki G. 2005. Developmental emergence of hippocampal fast-field "ripple" oscillations in the behaving rat pups. Neuroscience 134:1423–1430. DOI: https://doi.org/10.1016/j.neuroscience.2005.05.030, PMID: 16039793
Buzsáki G. 2015. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–1188. DOI: https://doi.org/10.1002/hipo.22488, PMID: 26135716
Cichon NB, Denker M, Grün S, Hanganu-Opatz IL. 2014. Unsupervised classification of neocortical activity patterns in neonatal and pre-juvenile rodents. Frontiers in Neural Circuits 8:50. DOI: https://doi.org/10.3389/fncir.2014.00050, PMID: 24904296
Cirelli C, Tononi G. 2015. Cortical development, electroencephalogram rhythms, and the sleep/wake cycle. Biological Psychiatry 77:1071–1078. DOI: https://doi.org/10.1016/j.biopsych.2014.12.017, PMID: 25680672
Colgin LL. 2011. Oscillations and hippocampal-prefrontal synchrony. Current Opinion in Neurobiology 21:467– 474. DOI: https://doi.org/10.1016/j.conb.2011.04.006, PMID: 21571522
Colgin LL. 2016. Rhythms of the hippocampal network. Nature Reviews Neuroscience 17:239–249. DOI: https://doi.org/10.1038/nrn.2016.21, PMID: 26961163
Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW. 2009. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. PNAS 106:11794–11799. DOI: https://doi.org/10.1073/pnas. 0812608106, PMID: 19561297
Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ. 2006. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439:79–83. DOI: https://doi.org/10.1038/nature04264, PMID: 16327778
Eichenbaum H. 2017. Prefrontal-hippocampal interactions in episodic memory. Nature Reviews Neuroscience 18: 547–558. DOI: https://doi.org/10.1038/nrn.2017.74, PMID: 28655882
Fanselow MS, Dong HW. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19. DOI: https://doi.org/10.1016/j.neuron.2009.11.031, PMID: 20152109
Geisler C, Robbe D, Zugaro M, Sirota A, Buzsáki G. 2007. Hippocampal place cell assemblies are speed-controlled oscillators. PNAS 104:8149–8154. DOI: https://doi.org/10.1073/pnas.0610121104, PMID: 17470808
Granger CWJ. 1980. Testing for causality. Journal of Economic Dynamics and Control 2:329–352. DOI: https://doi.org/10.1016/0165-1889(80)90069-X
Hallock HL, Wang A, Griffin AL. 2016. Ventral midline thalamus is critical for hippocampal-prefrontal synchrony and spatial working memory. Journal of Neuroscience 36:8372–8389. DOI: https://doi.org/10.1523/JNEUROSCI.0991-16.2016, PMID: 27511010
Hanganu IL, Ben-Ari Y, Khazipov R. 2006. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. Journal of Neuroscience 26:6728–6736. DOI: https://doi.org/10.1523/JNEUROSCI.0752-06.2006, PMID: 16793 880
Hanganu-Opatz IL. 2010. Between molecules and experience: role of early patterns of coordinated activity for the development of cortical maps and sensory abilities. Brain Research Reviews 64:160–176. DOI: https://doi. org/10.1016/j.brainresrev.2010.03.005, PMID: 20381527
Hartung H, Brockmann MD, Pöschel B, De Feo V, Hanganu-Opatz IL. 2016. Thalamic and entorhinal network activity differently modulates the functional development of prefrontal-hippocampal interactions. The Journal of Neuroscience 36:3676–3690. DOI: https://doi.org/10.1523/JNEUROSCI.3232-15.2016, PMID: 27030754
Hoerder-Suabedissen A, Molnár Z. 2015. Development, evolution and pathology of neocortical subplate neurons. Nature Reviews Neuroscience 16:133–146. DOI: https://doi.org/10.1038/nrn3915, PMID: 25697157
Honeycutt JA, Keary Iii KM, Kania VM, Chrobak JJ. 2016. Developmental age differentially mediates the calcium-binding protein parvalbumin in the rat: Evidence for a selective decrease in hippocampal parvalbumin cell counts. Developmental Neuroscience 38:105–114. DOI: https://doi.org/10.1159/000444447, PMID: 27002731
Hu H, Vervaeke K, Storm JF. 2002. Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. The Journal of Physiology 545:783–805. DOI: https://doi.org/10.1113/jphysiol.2002.029249, PMID: 12482886
Hubel DH, Wiesel TN, LeVay S. 1977. Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society B: Biological Sciences 278:377–409. DOI: https://doi.org/10. 1098/rstb.1977.0050, PMID: 19791
Huberman AD, Speer CM, Chapman B. 2006. Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1. Neuron 52:247–254. DOI: https://doi.org/10.1016/j. neuron.2006.07.028, PMID: 17046688
Jay TM, Witter MP. 1991. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. The Journal of Comparative Neurology 313:574–586. DOI: https://doi.org/10.1002/cne.903130404, PMID: 1783682
Khazipov R, Minlebaev M, Valeeva G. 2013. Early gamma oscillations. Neuroscience 250:240–252. DOI: https://doi.org/10.1016/j.neuroscience.2013.07.019, PMID: 23872391
Krüger HS, Brockmann MD, Salamon J, Ittrich H, Hanganu-Opatz IL. 2012. Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats. Neurobiology of Learning and Memory 97:470–481. DOI: https://doi.org/10.1016/j.nlm.2012.04.001, PMID: 22521798
Lindemann C, Ahlbeck J, Bitzenhofer SH, Hanganu-Opatz IL. 2016. Spindle activity orchestrates plasticity during development and sleep. Neural Plasticity 2016:1–14. DOI: https://doi.org/10.1155/2016/5787423, PMID: 272 93903
Luhmann HJ, Khazipov R. 2018. Neuronal activity patterns in the developing barrel cortex. Neuroscience 368. DOI: https://doi.org/10.1016/j.neuroscience.2017.05.025, PMID: 28528963
Minlebaev M, Ben-Ari Y, Khazipov R. 2009. NMDA receptors pattern early activity in the developing barrel cortex in vivo. Cerebral Cortex 19:688–696. DOI: https://doi.org/10.1093/cercor/bhn115, PMID: 18663251
Minlebaev M, Colonnese M, Tsintsadze T, Sirota A, Khazipov R. 2011. Early γ oscillations synchronize developing thalamus and cortex. Science 334:226–229. DOI: https://doi.org/10.1126/science.1210574, PMID: 21998388
Moser MB, Moser EI, Forrest E, Andersen P, Morris RG. 1995. Spatial learning with a minislab in the dorsal hippocampus. PNAS 92:9697–9701. DOI: https://doi.org/10.1073/pnas.92.21.9697, PMID: 7568200
Moser EI, Krobert KA, Moser MB, Morris RG. 1998. Impaired spatial learning after saturation of long-term potentiation. Science 281:2038–2042. DOI: https://doi.org/10.1126/science.281.5385.2038, PMID: 9748165
Niwa M, Kamiya A, Murai R, Kubo K, Gruber AJ, Tomita K, Lu L, Tomisato S, Jaaro-Peled H, Seshadri S, Hiyama H, Huang B, Kohda K, Noda Y, O’Donnell P, Nakajima K, Sawa A, Nabeshima T. 2010. Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron 65:480–489. DOI: https://doi.org/10.1016/j.neuron.2010.01.019, PMID: 20188653
Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M. 2004. Identifying true brain interaction from EEG data using the imaginary part of coherency. Clinical Neurophysiology 115:2292–2307. DOI: https://doi.org/10.1016/j.clinph.2004.04.029, PMID: 15351371
O’Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map. New York: Oxford University Press.
O’Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330. DOI: https://doi.org/10.1002/hipo.450030307, PMID: 8353611
Patel J, Schomburg EW, Berényi A, Fujisawa S, Buzsáki G. 2013. Local generation and propagation of ripples along the septotemporal axis of the hippocampus. The Journal of Neuroscience 33:17029–17041. DOI: https://doi.org/10.1523/JNEUROSCI.2036-13.2013, PMID: 24155307
Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A. 2000. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Annals of the New York Academy of Sciences 911:369–391. DOI: https://doi.org/10.1111/j.1749-6632.2000.tb06738.x, PMID: 10911886
Place R, Farovik A, Brockmann M, Eichenbaum H. 2016. Bidirectional prefrontal-hippocampal interactions support context-guided memory. Nature Neuroscience 19:992–994. DOI: https://doi.org/10.1038/nn.4327, PMID: 27322417
Rodrigues PL, Baccala LA. 2016. Statistically significant time-varying neural connectivity estimation using generalized partial directed coherence. Conference proceedings: … Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Annual Conference 2016:5493–5496. DOI: https://doi.org/10.1109/EMBC.2016.7591970, PMID: 28269501
Royer S, Sirota A, Patel J, Buzsáki G. 2010. Distinct representations and theta dynamics in dorsal and ventral hippocampus. Journal of Neuroscience 30:1777–1787. DOI: https://doi.org/10.1523/JNEUROSCI.4681-09. 2010, PMID: 20130187
Seelke AM, Blumberg MS. 2010. Developmental appearance and disappearance of cortical events and oscillations in infant rats. Brain Research 1324:34–42. DOI: https://doi.org/10.1016/j.brainres.2010.01.088, PMID: 20138849
Shen J, Colonnese MT. 2016. Development of Activity in the Mouse Visual Cortex. Journal of Neuroscience 36: 12259–12275. DOI: https://doi.org/10.1523/JNEUROSCI.1903-16.2016, PMID: 27903733
Siapas AG, Wilson MA. 1998. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123–1128. DOI: https://doi.org/10.1016/S0896-6273(00)80629-7, PMID: 9856467
Siapas AG, Lubenov EV, Wilson MA. 2005. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141–151. DOI: https://doi.org/10.1016/j.neuron.2005.02.028, PMID: 15820700
Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA. 2010. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464:763–767. DOI: https://doi.org/10.1038/nature08855, PMID: 20360742
Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G. 2008. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683–697. DOI: https://doi.org/10.1016/j. neuron.2008.09.014, PMID: 19038224
Spellman T, Rigotti M, Ahmari SE, Fusi S, Gogos JA, Gordon JA. 2015. Hippocampal-prefrontal input supports spatial encoding in working memory. Nature 522:309–314. DOI: https://doi.org/10.1038/nature14445, PMID: 26053122
Stark E, Eichler R, Roux L, Fujisawa S, Rotstein HG, Buzsáki G. 2013. Inhibition-induced theta resonance in cortical circuits. Neuron 80:1263–1276. DOI: https://doi.org/10.1016/j.neuron.2013.09.033, PMID: 24314731
Stewart M, Fox SE. 1990. Do septal neurons pace the hippocampal theta rhythm? Trends in Neurosciences 13: 163–169. DOI: https://doi.org/10.1016/0166-2236(90)90040-H, PMID: 1693232
Strange BA, Witter MP, Lein ES, Moser EI. 2014. Functional organization of the hippocampal longitudinal axis. Nature Reviews Neuroscience 15:655–669. DOI: https://doi.org/10.1038/nrn3785, PMID: 25234264
Stujenske JM, Spellman T, Gordon JA. 2015. Modeling the spatiotemporal dynamics of light and heat propagation for in vivo optogenetics. Cell Reports 12:525–534. DOI: https://doi.org/10.1016/j.celrep.2015.06. 036, PMID: 26166563
Swanson LW. 1981. A direct projection from Ammon’s horn to prefrontal cortex in the rat. Brain Research 217: 150–154. DOI: https://doi.org/10.1016/0006-8993(81)90192-X, PMID: 7260612
Szczurkowska J, Cwetsch AW, dal Maschio M, Ghezzi D, Ratto GM, Cancedda L. 2016. Targeted in vivo genetic manipulation of the mouse or rat brain by in utero electroporation with a triple-electrode probe. Nature Protocols 11:399–412. DOI: https://doi.org/10.1038/nprot.2016.014, PMID: 26844428
Tabata H, Nakajima K. 2001. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865–872. DOI: https://doi.org/10.1016/S0306-4522(01)00016-1, PMID: 11301197
Taxidis J, Coomber B, Mason R, Owen M. 2010. Assessing cortico-hippocampal functional connectivity under anesthesia and kainic acid using generalized partial directed coherence. Biological Cybernetics 102:327–340. DOI: https://doi.org/10.1007/s00422-010-0370-1, PMID: 20204395
Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES. 2008. Genomic anatomy of the hippocampus. Neuron 60:1010–1021. DOI: https://doi.org/10.1016/j.neuron.2008.12.008, PMID: 19109908
Tolner EA, Sheikh A, Yukin AY, Kaila K, Kanold PO. 2012. Subplate neurons promote spindle bursts and thalamocortical patterning in the neonatal rat somatosensory cortex. Journal of Neuroscience 32:692–702. DOI: https://doi.org/10.1523/JNEUROSCI.1538-11.2012, PMID: 22238105
Vertes RP, Hoover WB, Szigeti-Buck K, Leranth C. 2007. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Research Bulletin 71:601–609. DOI: https://doi.org/10.1016/j.brainresbull.2006.12.002, PMID: 17292803
Wirt RA, Hyman JM. 2017. Integrating Spatial Working Memory and Remote Memory: Interactions between the Medial Prefrontal Cortex and Hippocampus. Brain Sciences 7:43. DOI: https://doi.org/10.3390/brainsci7040043, PMID: 28420200
Witter MP, Van Hoesen GW, Amaral DG. 1989. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. Journal of Neuroscience 9:216–228. PMID: 2913203
Witter MP, Amaral DG. 2004. Hippocampal Formation. In: The Rat Nervous System. Elsevier Inc. p. 635–704. DOI: https://doi.org/10.1016/B978-012547638-6/50022-5
Xu HP, Furman M, Mineur YS, Chen H, King SL, Zenisek D, Zhou ZJ, Butts DA, Tian N, Picciotto MR, Crair MC. 2011. An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 70:1115–1127. DOI: https://doi.org/10.1016/j.neuron.2011.04.028, PMID: 21689598
Xu W, Südhof TC. 2013. A neural circuit for memory specificity and generalization. Science 339:1290–1295. DOI: https://doi.org/10.1126/science.1229534, PMID: 23493706
Yang JW, Reyes-Puerta V, Kilb W, Luhmann HJ. 2016. Spindle bursts in neonatal rat cerebral cortex. Neural Plasticity 2016:1–11. DOI: https://doi.org/10.1155/2016/3467832, PMID: 27034844
Yasuda M, Johnson-Venkatesh EM, Zhang H, Parent JM, Sutton MA, Umemori H. 2011. Multiple forms of activity-dependent competition refine hippocampal circuits in vivo. Neuron 70:1128–1142. DOI: https://doi. org/10.1016/j.neuron.2011.04.027, PMID: 21689599
Ye X, Kapeller-Libermann D, Travaglia A, Inda MC, Alberini CM. 2017. Direct dorsal hippocampal-prelimbic cortex connections strengthen fear memories. Nature Neuroscience 20:52–61. DOI: https://doi.org/10.1038/nn.4443, PMID: 27869801
Yuste R, Nelson DA, Rubin WW, Katz LC. 1995. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14:7–17. DOI: https://doi.org/10.1016/0896-6273(95)90236-8, PMID: 7826643
Zhang L, Spigelman I, Carlen PL. 1990. Whole-cell patch study of GABAergic inhibition in CA1 neurons of immature rat hippocampal slices. Developmental Brain Research 56:127–130. DOI: https://doi.org/10.1016/0165-3806(90)90171-T, PMID: 2279324