Skip to main content

Computing Temporal Sequence with Dendrites

  • Chapter
  • First Online:
Book cover The Computing Dendrite

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 11))

  • 2152 Accesses

Abstract

This chapter describes recent experimental results showing that dendrites of cortical pyramidal neurons can compute the temporal sequence of synaptic input. Electrophysiological recordings combined with two-photon glutamate uncaging, calcium imaging, and compartmental modeling have shown that single cortical dendrites have a gradient of nonlinear synaptic integration, which relies on dendritic impedance gradients and nonlinear synaptic NMDA receptor activation. This gradient confers high sensitivity to the temporal input sequence, allowing single dendrites and individual neurons to implement a fundamental cortical computation.

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

  • Agmon-Snir H, Carr CE, Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393(6682):268–272

    Article  PubMed  CAS  Google Scholar 

  • Barlow HB, Levick WR (1965) The mechanism of directionally selective units in rabbit's retina. J Physiol 178(3):477–504

    PubMed  CAS  Google Scholar 

  • Borg-Graham LJ, Grzywacz NM (1992) A model of the directional selectivity circuit in retina: transformations by neurons singly and in concert. In: McKenna T, Davis J, Zornetzer ZF (eds) Single neuron computation. Academic, San Diego, pp 347–376

    Google Scholar 

  • Branco T, Häusser M (2010) The single dendritic branch as a fundamental functional unit in the nervous system. Curr Opin Neurobiol 20(4):494–502

    Article  PubMed  CAS  Google Scholar 

  • Branco T, Häusser M (2011) Synaptic integration gradients in single cortical pyramidal cell dendrites. Neuron 69(5):885–892

    Article  PubMed  CAS  Google Scholar 

  • Branco T, Clark BA, Häusser M (2010) Dendritic discrimination of temporal input sequences in cortical neurons. Science 329(5999):1671–1675

    Article  PubMed  CAS  Google Scholar 

  • deCharms RC, Merzenich MM (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381(6583):610–613

    Article  PubMed  CAS  Google Scholar 

  • DiGregorio DA, Rothman JS, Nielsen TA, Silver RA (2007) Desensitization properties of AMPA receptors at the cerebellar mossy fiber granule cell synapse. J Neurosci 27(31):8344–8357

    Article  PubMed  CAS  Google Scholar 

  • Ellis-Davies GC (2007) Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nat Methods 4(8):619–628

    Article  PubMed  CAS  Google Scholar 

  • Euler T, Detwiler PB, Denk W (2002) Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418(6900):845–852

    Article  PubMed  CAS  Google Scholar 

  • Faisal AA, Laughlin SB (2007) Stochastic simulations on the reliability of action potential propagation in thin axons. PLoS Comput Biol 3(5):e79

    Article  PubMed  Google Scholar 

  • Golding NL, Spruston N (1998) Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21(5):1189–1200

    Article  PubMed  CAS  Google Scholar 

  • Gulledge AT, Kampa BM, Stuart GJ (2005) Synaptic integration in dendritic trees. J Neurobiol 64(1):75–90

    Article  PubMed  CAS  Google Scholar 

  • Hausselt SE, Euler T, Detwiler PB, Denk W (2007) A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol 5(7):e185

    Article  PubMed  Google Scholar 

  • Helmstaedter M, de Kock CP, Feldmeyer D, Bruno RM, Sakmann B (2007) Reconstruction of an average cortical column in silico. Brain Res Rev 55(2):193–203

    Article  PubMed  CAS  Google Scholar 

  • Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7(2):170–177

    Article  PubMed  CAS  Google Scholar 

  • Johnston D, Narayanan R (2008) Active dendrites: colorful wings of the mysterious butterflies. Trends Neurosci 31(6):309–316

    Article  PubMed  CAS  Google Scholar 

  • Katz Y, Menon V, Nicholson DA, Geinisman Y, Kath WL, Spruston N (2009) Synapse distribution suggests a two-stage model of dendritic integration in CA1 pyramidal neurons. Neuron 63(2):171–177

    Article  PubMed  CAS  Google Scholar 

  • Larkman AU, Major G, Stratford KJ, Jack JJ (1992) Dendritic morphology of pyramidal neurones of the visual cortex of the rat. IV: electrical geometry. J Comp Neurol 323(2):137–152

    Article  PubMed  CAS  Google Scholar 

  • Larkum ME, Waters J, Sakmann B, Helmchen F (2007) Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. J Neurosci 27(34):8999–9008

    Article  PubMed  CAS  Google Scholar 

  • Lester RA, Jahr CE (1992) NMDA channel behavior depends on agonist affinity. J Neurosci 12(2):635–643

    PubMed  CAS  Google Scholar 

  • Little JP, Carter AG (2012) Subcellular synaptic connectivity of layer 2 pyramidal neurons in the medial prefrontal cortex. J Neurosci 32(37):12808–12819

    Article  PubMed  CAS  Google Scholar 

  • Livingstone MS (1998) Mechanisms of direction selectivity in macaque V1. Neuron 20(3):509–526

    Article  PubMed  CAS  Google Scholar 

  • London M, Häusser M (2005) Dendritic computation. Annu Rev Neurosci 28:503–532

    Article  PubMed  CAS  Google Scholar 

  • Lörincz A, Notomi T, Tamás G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5(11):1185–1193

    Article  PubMed  Google Scholar 

  • Losonczy A, Magee JC (2006) Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50(2):291–307

    Article  PubMed  CAS  Google Scholar 

  • Magee JC (1999) Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2(6):508–514

    Article  PubMed  CAS  Google Scholar 

  • Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1(3):181–190

    Article  PubMed  CAS  Google Scholar 

  • Magee JC, Cook EP (2000) Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3(9):895–903

    Article  PubMed  CAS  Google Scholar 

  • Major G, Polsky A, Denk W, Schiller J, Tank DW (2008) Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J Neurophysiol 99(5):2584–2601

    Article  PubMed  CAS  Google Scholar 

  • Mathews PJ, Jercog PE, Rinzel J, Scott LL, Golding NL (2010) Control of submillisecond synaptic timing in binaural coincidence detectors by K(v)1 channels. Nat Neurosci 13(5):601–609

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4(11):1086–1092

    Article  PubMed  CAS  Google Scholar 

  • Mayer ML, Westbrook GL, Guthrie PB (1984) Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309(5965):261–263

    Article  PubMed  CAS  Google Scholar 

  • Meister M, Lagnado L, Baylor DA (1995) Concerted signaling by retinal ganglion cells. Science 270(5239):1207–1210

    Article  PubMed  CAS  Google Scholar 

  • Mel BW (1993) Synaptic integration in an excitable dendritic tree. J Neurophysiol 70(3):1086–1101

    PubMed  CAS  Google Scholar 

  • Nevian T, Larkum ME, Polsky A, Schiller J (2007) Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat Neurosci 10(2):206–214

    Article  PubMed  CAS  Google Scholar 

  • Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307(5950):462–465

    Article  PubMed  CAS  Google Scholar 

  • Petreanu L, Mao T, Sternson SM, Svoboda K (2009) The subcellular organization of neocortical excitatory connections. Nature 457(7233):1142–1145

    Article  PubMed  CAS  Google Scholar 

  • Poirazi P, Brannon T, Mel BW (2003) Pyramidal neuron as two-layer neural network. Neuron 37(6):989–999

    Article  PubMed  CAS  Google Scholar 

  • Rall W (1964) Theoretical significance of dendritic trees for neuronal input–output relations. In: Reiss R (ed) Neural theory and modeling. Stanford Univ. Press, Stanford, CA, pp 73–97

    Google Scholar 

  • Richardson RJ, Blundon JA, Bayazitov IT, Zakharenko SS (2009) Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex. J Neurosci 29(20):6406–6417

    Article  PubMed  CAS  Google Scholar 

  • Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol 505(Pt 3):605–616

    Article  PubMed  CAS  Google Scholar 

  • Schiller J, Major G, Koester HJ, Schiller Y (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404(6775):285–289

    Article  PubMed  CAS  Google Scholar 

  • Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41(3):798–820

    PubMed  CAS  Google Scholar 

  • Watts J, Thomson AM (2005) Excitatory and inhibitory connections show selectivity in the neocortex. J Physiol 562(Pt 1):89–97

    Article  PubMed  CAS  Google Scholar 

  • Wehr M, Laurent G (1996) Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384(6605):162–166

    Article  PubMed  CAS  Google Scholar 

  • Williams SR, Stuart GJ (2000) Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol 83(5):3177–3182

    PubMed  CAS  Google Scholar 

  • Zador AM, Agmon-Snir H, Segev I (1995) The morphoelectrotonic transform: a graphical approach to dendritic function. J Neurosci 15(3 Pt 1):1669–1682

    PubMed  CAS  Google Scholar 

  • Zhang LI, Tan AY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424(6945):201–205

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiago Branco .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Branco, T. (2014). Computing Temporal Sequence with Dendrites. In: Cuntz, H., Remme, M., Torben-Nielsen, B. (eds) The Computing Dendrite. Springer Series in Computational Neuroscience, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8094-5_15

Download citation

Publish with us

Policies and ethics