Skip to main content

Voltage Imaging in the Study of Hippocampal Circuit Function and Plasticity

  • Chapter
Membrane Potential Imaging in the Nervous System and Heart

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 859))

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aihara T, Kobayashi Y, Tsukada M (2005) Spatiotemporal visualization of long-term potentiation and depression in the hippocampal CA1 area. Hippocampus 15:68–78

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Buckmaster PS, Schwartzkroin PA (1994) Hippocampal mossy cell function: a speculative view. Hippocampus 4:393–402

    Article  CAS  PubMed  Google Scholar 

  • Cao G, Platisa J, Pieribone VA, Raccuglia D, Kunst M, Nitabach MN (2013) Genetically targeted optical electrophysiology in intact neural circuits. Cell

    Google Scholar 

  • Chang PY, Jackson MB (2006a) Heterogeneous spatial patterns of long-term potentiation in rat hippocampal slices. J Physiol 576:427–443

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Claiborne BJ, Xiang Z, Brown TH (1993) Hippocampal circuitry complicates analysis of long-term potentiation in mossy fiber synapses. Hippocampus 3:115–121

    Article  CAS  PubMed  Google Scholar 

  • Colgin LL, Moser EI, Moser MB (2008) Understanding memory through hippocampal remapping. Trends Neurosci 31:469–477

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Dudek FE, Sutula TP (2007) Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res 163:755–773

    Article  CAS  PubMed  Google Scholar 

  • Gerstner W, Abbott LF (1997) Learning navigational maps through potentiation and modulation of hippocampal place cells. J Comput Neurosci 4:79–94

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Henze DA, Buzsaki G (2007) Hilar mossy cells: functional identification and activity in vivo. Prog Brain Res 163:199–216

    Article  PubMed  Google Scholar 

  • Hitti FL, Siegelbaum SA (2014) The hippocampal CA2 region is essential for social memory. Nature 508:88–92

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Hsu D (2007) The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res 163:601–613

    Article  PubMed  Google Scholar 

  • Jackson MB (2013) Recall of spatial patterns stored in a hippocampal slice by long-term potentiation. J Neurophysiol 110(11):2511–2519

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kesner RP, Gilbert PE, Wallenstein GV (2000) Testing neural network models of memory with behavioral experiments. Curr Opin Neurobiol 10:260–265

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Leutgeb S, Leutgeb JK (2007) Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem 14:745–757

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84:87–136

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31:69–89

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rolls ET (2013) The mechanisms for pattern completion and pattern separation in the hippocampus. Front Syst Neurosci 7:74

    Article  PubMed Central  PubMed  Google Scholar 

  • Rolls ET, Treves A (1994) Neural networks in the brain involved in memory and recall. Prog Brain Res 102:335–341

    Article  CAS  PubMed  Google Scholar 

  • Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, Oxford

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Scharfman HE (1995) Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J Neurophysiol 74:179–194

    CAS  PubMed  Google Scholar 

  • Scharfman HE, Myers CE (2013) Hilar mossy cells of the dentate gyrus: a historical perspective. Front Neural Circuits 6:106

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang D, Zhang Z, Chanda B, Jackson MB (2010) Improved probes for hybrid voltage sensor imaging. Biophys J 99:2355–2365

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wright BJ, Jackson MB (2014) Long-term potentiation in hilar circuitry modulates gating by the dentate gyrus. J Neurosci 34:9743–9753

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515–525

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Meyer B. Jackson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics