Abstract
Recurrent inhibitory loops are simple neuronal circuits found in the central nervous system, yet little is known about the physiological rules governing their activity. Here we use simultaneous somatic and dendritic recordings in rat hippocampal slices to show that during a series of action potentials in pyramidal cells recurrent inhibition rapidly shifts from their soma to the apical dendrites. Two distinct inhibitory circuits are sequentially recruited to produce this shift: one, time-locked with submillisecond precision to the onset of the action potential series, transiently inhibits the somatic and perisomatic regions of pyramidal cells; the other, activated in proportion to the rate of action potentials in the series, durably inhibits the distal apical dendrites. These two operating modes result from the synergy between pre- and postsynaptic properties of excitatory synapses onto recurrent inhibitory neurons with distinct projection patterns. Thus, the onset of a series of action potentials and the rate of action potentials in the series are selectively captured and transformed into different spatial patterns of recurrent inhibition.
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References
Adrian, E. D. The Basis of Sensation: The Action of the Sense Organs (W. W. Norton, New York, 1928)
Rieke, F., Warland, D., de Ruyter van Steveninck, R. & Bialek, W. Spikes: Exploring the Neural Code (The MIT Press, Cambridge, Massachusetts/London, UK, 1997)
Dayan, P. & Abbott, L. F. Theoretical Neurosciences: Computational and Mathematical Modeling of Neural Systems (The MIT Press, Cambridge, Massachusetts/London, UK, 2001)
Andersen, P., Eccles, J. C. & Loyning, Y. Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 198, 540–542 (1963)
Megias, M., Emri, Z., Freund, T. F. & Gulyas, A. I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527–540 (2001)
Stuart, G. J., Dodt, H. U. & Sakmann, B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch. 423, 511–518 (1993)
Spruston, N., Schiller, Y., Stuart, G. & Sakmann, B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268, 297–300 (1995)
Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159–1160 (2001)
Kandel, E. R., Spencer, W. A. & Brinley, F. J. Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J. Neurophysiol. 24, 225–242 (1961)
Dingledine, R. & Langmoen, I. A. Conductance changes and inhibitory actions of hippocampal recurrent IPSPs. Brain Res. 185, 277–287 (1980)
Alger, B. E. & Nicoll, R. A. Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro. J. Physiol. 328, 105–123 (1982)
Maccaferri, G. & McBain, C. J. Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15, 137–145 (1995)
Pearce, R. A. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10, 189–200 (1993)
Spruston, N., Jaffe, D. B., Williams, S. H. & Johnston, D. Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70, 781–802 (1993)
Freund, T. F. & Buzsáki, G. Interneurons of the hippocampus. Hippocampus 6, 347–470 (1996)
Geiger, J. R. P., Lubke, J., Roth, A., Frotscher, M. & Jonas, P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009–1023 (1997)
Fricker, D. & Miles, R. EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28, 559–569 (2000)
Ali, A. B. & Thomson, A. M. Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J. Physiol. 507.1, 185–199 (1998)
Ali, A. B., Deuchars, J., Pawelzik, H. & Thomson, A. M. CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J. Physiol. 507.1, 201–219 (1998)
Shigemoto, R. et al. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381, 523–525 (1996)
Scanziani, M., Gahwiler, B. H. & Charpak, S. Target cell-specific modulation of transmitter release at terminals from a single axon. Proc. Natl Acad. Sci. USA 95, 12004–12009 (1998)
Toth, K., Suares, G., Lawrence, J. J., Philips-Tansey, E. & McBain, C. J. Differential mechanisms of transmission at three types of mossy fiber synapse. J. Neurosci. 20, 8279–8289 (2000)
Losonczy, A., Zhang, L., Shigemoto, R., Somogyi, P. & Nusser, Z. Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones. J. Physiol. 542, 193–210 (2002)
Buhl, E. H., Szilagyi, T., Halasy, K. & Somogyi, P. Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus in vitro. Hippocampus 6, 294–305 (1996)
Gulyás, A. I., Megias, M., Emri, Z. & Freund, T. F. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci. 19, 10082–10097 (1999)
Banks, M. I., White, J. A. & Pearce, R. A. Interactions between distinct GABA(A) circuits in hippocampus. Neuron 25, 449–457 (2000)
Arai, A. C., Xia, Y.-F., Rogers, G., Lynch, G. & Kessler, M. Benzamide-type AMPA receptor modulators form two subfamilies with distinct modes of action. J. Pharmacol. Exp. Ther. 303, 1075–1085 (2002)
Klausberger, T. et al. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844–849 (2003)
O'Keefe, J. & Recce, M. L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993)
Somogyi, P., Tamas, G., Lujan, R. & Buhl, E. H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26, 113–135 (1998)
Beierlein, M., Gibson, J. R. & Connors, B. W. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987–3000 (2003)
Acknowledgements
We thank B. Gähwiler from the Brain Research Institute of the University of Zürich, where the initial part of the study was performed. We thank J. Anderson for instructions on the use of the camera lucida. We also thank U. Gerber and M. Carandini for critical reading of and L. Glickfeld for comments on the manuscript. This work was supported by the Swiss National Science Foundation and NIH grants.
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Supplementary information
Supplementary Methods
Experimental protocols used to test the specificity of Alveus stimulation and to recover the morphology of recorded interneurons. (DOC 21 kb)
Supplementary Figure 1
Recurrent IPSPs are not contaminated by feed-forward IPSPs. (PDF 49 kb)
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Pouille, F., Scanziani, M. Routing of spike series by dynamic circuits in the hippocampus. Nature 429, 717–723 (2004). https://doi.org/10.1038/nature02615
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DOI: https://doi.org/10.1038/nature02615
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