Abstract
Synaptic plasticity has the capacity to alter the function of neural circuits, and long-term potentiation (LTP) of synaptic transmission induced by high frequency electrical activity has the capacity to store information in neural circuits. The cellular and molecular mechanisms of LTP have been studied intensively for many years and much progress has been made on this front. By contrast, how synaptic plasticity alters circuit function has received much less attention and remains poorly understood. Voltage imaging provides a powerful general technique for the study of neural circuitry, and studies of synaptic plasticity with voltage imaging are beginning to reveal important aspects of how the function of a neural circuit can change when the strength of its synapses has been modified. The hippocampus has an important role in learning and memory and the plasticity of its synapses has received much attention. Voltage imaging with voltage sensitive dye in the CA1 region of a hippocampal slice has shown that spatial patterns of enhancement following LTP induction can diverge from the spatial patterns elicited by electrical stimulation, suggesting that LTP exhibits a distinct organizational structure. LTP can alter the throughput of electrical activity in the dentate gyrus of a hippocampal slice, to gate transmission on to the CA3 region. The spatial patterns evoked by complex electrical stimulation can be stored within the CA3 region in a hippocampal slice, allowing patterns to be reconstructed with simpler electrical stimulation. Thus, voltage imaging has demonstrated that the CA3 circuit has the capacity for pattern completion. These studies with voltage sensitive dye illustrate a range of interesting and novel questions that can be addressed at the population level. It is hoped that future imaging experiments with single-cell resolution using genetically-encoded voltage sensors will provide a more detailed picture of how synaptic plasticity modifies the information processing capabilities of neural circuits.
Keywords
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Aihara T, Kobayashi Y, Tsukada M (2005) Spatiotemporal visualization of long-term potentiation and depression in the hippocampal CA1 area. Hippocampus 15:68–78
Amaral DG, Lavenex P (2007) Hippocampal neuroanatomy. In: Andersen P, Morris R, Amaral DG, Bliss TV, O'Keefe J (eds) The hippocampus book. Oxford University Press, Oxford, pp 37–114
Ang CW, Carlson GC, Coulter DA (2006) Massive and specific dysregulation of direct cortical input to the hippocampus in temporal lobe epilepsy. J Neurosci 26:11850–11856
Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232:357–374
Buckmaster PS, Schwartzkroin PA (1994) Hippocampal mossy cell function: a speculative view. Hippocampus 4:393–402
Cao G, Platisa J, Pieribone VA, Raccuglia D, Kunst M, Nitabach MN (2013) Genetically targeted optical electrophysiology in intact neural circuits. Cell
Chang PY, Jackson MB (2006a) Heterogeneous spatial patterns of long-term potentiation in rat hippocampal slices. J Physiol 576:427–443
Chang PY, Jackson MB (2006b) Heterogeneous spatial patterns of long-term potentiation in hippocampal slices. Department of Biophysics. University of Wisconsin, Madison, WI, p 144
Chang PY, Taylor PE, Jackson MB (2007) Voltage imaging reveals the CA1 region at the CA2 border as a focus for epileptiform discharges and long-term potentiation in hippocampal slices. J Neurophysiol 98:1309–1322
Claiborne BJ, Xiang Z, Brown TH (1993) Hippocampal circuitry complicates analysis of long-term potentiation in mossy fiber synapses. Hippocampus 3:115–121
Colgin LL, Moser EI, Moser MB (2008) Understanding memory through hippocampal remapping. Trends Neurosci 31:469–477
de Almeida L, Idiart M, Lisman JE (2007) Memory retrieval time and memory capacity of the CA3 network: role of gamma frequency oscillations. Learn Mem 14:795–806
Dudek FE, Sutula TP (2007) Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res 163:755–773
Gerstner W, Abbott LF (1997) Learning navigational maps through potentiation and modulation of hippocampal place cells. J Comput Neurosci 4:79–94
Gong Y, Wagner MJ, Zhong Li J, Schnitzer MJ (2014) Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat Commun 5:3674
Ghitani N, Bayguinov BO, Ma Y, Jackson MB (2015) Single-trial imaging of spikes and synaptic potentials in single neurons in brain slices with genetically-encoded hybrid voltage sensor. J Neurophysiol 113:1249–1259
Heinemann U, Beck H, Dreier JP, Ficker E, Stabel J, Zhang CL (1992) The dentate gyrus as a regulated gate for the propagation of epileptiform activity. Epilepsy Res Suppl 7:273–280
Henze DA, Buzsaki G (2007) Hilar mossy cells: functional identification and activity in vivo. Prog Brain Res 163:199–216
Hitti FL, Siegelbaum SA (2014) The hippocampal CA2 region is essential for social memory. Nature 508:88–92
Hosokawa T, Ohta M, Saito T, Fine A (2003) Imaging spatio-temporal patterns of long-term potentiation in mouse hippocampus. Philos Trans R Soc Lond B Biol Sci 358:689–693
Hsu D (2007) The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res 163:601–613
Jackson MB (2013) Recall of spatial patterns stored in a hippocampal slice by long-term potentiation. J Neurophysiol 110(11):2511–2519
Jackson MB, Scharfman HE (1996) Positive feedback from hilar mossy cells to granule cells in the dentate gyrus revealed by voltage-sensitive dye and microelectrode recording. J Neurophysiol 76:601–616
Kesner RP, Gilbert PE, Wallenstein GV (2000) Testing neural network models of memory with behavioral experiments. Curr Opin Neurobiol 10:260–265
Kleschevnikov AM, Routtenberg A (2003) Long-term potentiation recruits a trisynaptic excitatory associative network within the mouse dentate gyrus. Eur J Neurosci 17:2690–2702
Leutgeb S, Leutgeb JK (2007) Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem 14:745–757
Lothman EW, Stringer JL, Bertram EH (1992) The dentate gyrus as a control point for seizures in the hippocampus and beyond. Epilepsy Res Suppl 7:301–313
Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84:87–136
Lysetskiy M, Foldy C, Soltesz I (2005) Long- and short-term plasticity at mossy fiber synapses on mossy cells in the rat dentate gyrus. Hippocampus 15:691–696
Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711
McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94–99
McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415
Momose-Sato Y, Sato K, Arai Y, Yazawa I, Mochida H, Kamino K (1999) Evaluation of voltage-sensitive dyes for long-term recording of neural activity in the hippocampus. J Membr Biol 172:145–157
Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31:69–89
Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188–201
Neves G, Cooke SF, Bliss TV (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9:65–75
Niewoehner B, Single FN, Hvalby O, Jensen V, Meyerzum Alten Borgloh S, Seeburg PH, Rawlins JN, Sprengel R, Bannerman DM (2007) Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur J Neurosci 25:837–846
Rolls ET (2013) The mechanisms for pattern completion and pattern separation in the hippocampus. Front Syst Neurosci 7:74
Rolls ET, Treves A (1994) Neural networks in the brain involved in memory and recall. Prog Brain Res 102:335–341
Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, Oxford
Saggau P, Galvan M, ten Bruggencate G (1986) Long-term potentiation in guinea pig hippocampal slices monitored by optical recording of neuronal activity. Neurosci Lett 69:53–58
Scharfman HE (1995) Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J Neurophysiol 74:179–194
Scharfman HE, Myers CE (2013) Hilar mossy cells of the dentate gyrus: a historical perspective. Front Neural Circuits 6:106
Scharfman HE, Kunkel DD, Schwartzkroin PA (1990) Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37:693–707
St-Pierre F, Marshall JD, Yang Y, Gong Y, Schnitzer MJ, Lin MZ (2014) High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci 17:884–889
Wang D, Zhang Z, Chanda B, Jackson MB (2010) Improved probes for hybrid voltage sensor imaging. Biophys J 99:2355–2365
Wright BJ, Jackson MB (2014) Long-term potentiation in hilar circuitry modulates gating by the dentate gyrus. J Neurosci 34:9743–9753
Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515–525
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Wright, B.J., Jackson, M.B. (2015). Voltage Imaging in the Study of Hippocampal Circuit Function and Plasticity. In: Canepari, M., Zecevic, D., Bernus, O. (eds) Membrane Potential Imaging in the Nervous System and Heart. Advances in Experimental Medicine and Biology, vol 859. Springer, Cham. https://doi.org/10.1007/978-3-319-17641-3_8
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DOI: https://doi.org/10.1007/978-3-319-17641-3_8
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