Skip to main content
SpringerLink
Log in

Differential dynamics of transient neuronal assemblies in visual compared to auditory cortex

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Large-scale, coherent, but highly transient networks of neurons, ‘neuronal assemblies’, operate over a sub-second time frame. Such assemblies of brain cells need not necessarily respect well-defined anatomical compartmentalisation, but represent an intermediate level of brain organisation between identified brain regions and individual neurons dependent on the activity status of the synaptic connections and axonal projections. To study neuronal assemblies both in slices and in the living brain, optical imaging using voltage-sensitive dyes (VSDI) offers the highest spatial and temporal resolution in real-time. Applying VSDI technique to compare assemblies in visual versus auditory cortices under standardised experimental protocols, we observed no significant variations in the basic parameters of fluorescence signal and assembly size: such results might be predicted from the canonical invariance of cortical structures across modalities. However, further analysis revealed less obvious yet significant differences in the assembly dynamics of the two regions. The neural assemblies spread widely across layers in the two cortices following paired-pulse stimulation of putative layer 4. The respective patterns of activity started to differentiate within a specific time frame (250–300 ms). The signal was predominant near the point of stimulation in the visual cortex, whereas in the auditory cortex the signal was stronger in the superficial layers. This modality-specific divergence in assembly dynamics highlights a previously under-appreciated level of neuronal processing. Additionally, these findings could prompt a new approach to the understanding of how information from different senses, transmitted as action potentials with identical electrochemical characteristics across different cortices, be it visual or auditory, can eventually yield, nonetheless, the qualitatively distinct experiences of seeing or hearing.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Brodmann K (1909) Vergleichende localisationslehre der grosshirnrinde in ihren principien dargestellt auf grund des zellenbaues. (Leipzig: Barth) [Trans Garey, L.J. Brodmann’s localisation in the Cerebral Cortex (London: Smith-Gordon, 1994)]

  • Bronchti G, Heil P, Sadka R, Scheich H, Wollberg Z (2002) Auditory activation of “visual” cortical areas in the blind mole rat (Spalax ehrenbergi). Eur J Neurosci 16:311–329

    Article  PubMed  Google Scholar 

  • Burton H (2003) Visual cortex activity in early and late blind people. J Neurosci 23:4005–4011

    PubMed  CAS  Google Scholar 

  • Chalmers DJ (1998) In: Hameroff S, Kaszniak A, Scott A (eds) On the Search for the Neural Correlate of Consciousness. Toward a Science of Consciousness II. MIT Press, Cambridge

  • Cohen LB, Salzberg BM, Grinvald A (1978) Optical methods for monitoring neuron activity. Annu Rev Neurosci 1:171–182

    Article  PubMed  CAS  Google Scholar 

  • Collins TF, Mann EO, Hill MRH, Dommet EJ, Greenfield SA (2007) Dynamics of neuronal assemblies are modulated by anesthetics but not analgesics. Eur J Anaesth (in press)

  • Cooper HM, Herbin M, Nevo E (1993) Visual system of a naturally micropthlamic mammal: the blind mole rat (Spalax ehrenbergi). J Comp Neurol 328:13–350

    Article  Google Scholar 

  • Debanne D, Guérineau NC, Gähwiler BH, Thompson SM (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 15:163–176

    Google Scholar 

  • Douglas RJ, Martin KAC (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27:419–451

    Article  PubMed  CAS  Google Scholar 

  • Ehret G (1997) The auditory cortex. J Comp Physiol A 181:547–557

    Article  PubMed  CAS  Google Scholar 

  • Greenfield SA, Collins TFT (2005) A neuroscientific approach to consciousness. Prog Brain Res 150:11–23

    Article  PubMed  Google Scholar 

  • Grinvald A (1985) Real-time optical mapping of neuronal activity: from single growth cones to the intact mammalian brain. Annu Rev Neurosci 8:263–305

    Article  PubMed  CAS  Google Scholar 

  • Grinvald A, Hildesheim R (2004) VSDI: a new era in functional imaging of cortical dynamics. Nat Rev Neurosci 5:874–875

    Article  PubMed  CAS  Google Scholar 

  • Grinvald A, Anglister L, Freeman JA, Hildesheim R, Manker A (1984) Real-time optical imaging of naturally evoked electrical activity in intact frog brain. Nature 308:848–850

    Article  PubMed  CAS  Google Scholar 

  • Grinvald A, Shoham D, Shmuel A, Glaser DE, Vanzetta I, Shtoyerman E, Slovin H, Sterkin A, Wijnbergen C, Hildesheim R, Arieli A (1999) In-vivo optical imaging of cortical architecture and dynamics. In: T Windhorst H Johansson (eds) Modern techniques in neuroscience research. Springer, Heidelberg pp 893–969

    Google Scholar 

  • Huang CL, Winer JA (2000) Auditory thalamocortical projections in the cat laminar and areal patterns of input. J Comp Neurol 427:302–331

    Article  PubMed  CAS  Google Scholar 

  • Hunt DL, Yamoah EN, Krubitzer L (2006) Multisensory plasticity in congenitally deaf mice: How are cortical areas functionally specified? Neuroscience 139:1507–1524

    Article  PubMed  CAS  Google Scholar 

  • Heil P, Bronchti G, Wollberg Z, Scheich H (1991) Invasion of visual cortex by the auditory system in the naturally blind mole rat. Neuroreport 2:735–738

    Article  PubMed  CAS  Google Scholar 

  • Jung JC, Mehta AD, Aksay E, Stenoski R, Schnitzer MJ (2004) In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy. J Neurophysiol 92:3121–3133

    Article  PubMed  Google Scholar 

  • Kaas JH, Collins CE (2001) The organization of sensory cortex. Curr Opin Neurobiol 11:498–504

    Article  PubMed  CAS  Google Scholar 

  • Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195:481–492

    PubMed  CAS  Google Scholar 

  • Kerssens C, Klein J, van der Woerd A, Bonke B (2001) Auditory information processing during adequate propofol anesthesia monitored by electroencephalogram bispectral index. Anesth Analg 92:1210–1214

    Article  PubMed  CAS  Google Scholar 

  • Krubitzer L (1995) The organization of neocortex in mammals: are species differences really so different? Trends Neurosci 18:408–417

    Article  PubMed  CAS  Google Scholar 

  • Krubitzer L, Kaas JH (2005) The evolution of neocortex in mammals: how is phenotypic diversity generated? Curr Opin Neurobiol 15:444–453

    Article  PubMed  CAS  Google Scholar 

  • LeVay S, Gilbert CD (1976) Laminar patterns of geniculocortical projection in the cat. Brain Res 113:1–19

    Article  PubMed  CAS  Google Scholar 

  • Linden J, Schreiner CE (2003) Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cer Cor 13:83–89

    Article  Google Scholar 

  • Lubke GH, Kerssens C, Phaf H, Sebel PS (1999) Dependence of explicit and implicit memory on hypnotic state in trauma patients. Anesthesia 90:1–12

    Article  Google Scholar 

  • Mann EO, Tominaga T, Ichikawa M, Greenfield SA (2005) Cholinergic modulation of the spatiotemporal pattern of hippocampal activity and plasticity in vitro. Neuropharm 48:118–133

    Article  CAS  Google Scholar 

  • Mehta AD, Jung JC, Flusberg BA, Schnitzer MJ (2004) Fiber optic in vivo imaging in the mammalian nervous system. Curr Opin Neurobiol 14:617–628

    Article  PubMed  CAS  Google Scholar 

  • Metzinger T (2000) In neural correlates of consciousness: empirical and conceptual questions. MIT Press, Cambridge

    Google Scholar 

  • Mountcastle VB (1997) The columnar organisation of the neocortex. Brain 120:701–722

    Article  PubMed  Google Scholar 

  • Neville H, Jschmidt A, Kutas M (1983) Altered visual-evoked potentials in congenitally deaf adults. Brain Res 266:127–132

    Article  PubMed  CAS  Google Scholar 

  • Orbach HS, Cohen LB, Grinvald A (1985) Optical mapping of electrical activity in rat somatosensory and visual cortex. J Neurosci 5:1886–1895

    PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic, California

    Google Scholar 

  • Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in the structure of the neocortex. Brain 103:221–244

    Article  PubMed  CAS  Google Scholar 

  • Rockland KS (1998) Complex microstructures of sensory cortical connections. Curr Opin Neurobiol 8:545–551

    Article  PubMed  CAS  Google Scholar 

  • Roe AW, Pallas SL, Hahm J-O, Sur M (1990) A map of visual cortex induced in primary auditory cortex. Science 250:818–820

    Article  PubMed  CAS  Google Scholar 

  • Sadato N, Pascual-Leone A, Grafman J, Deiber MP, Ibanez V, Hallett M (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380:526–528

    Article  PubMed  CAS  Google Scholar 

  • Shoham D., Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, Grinvald A (1999) Imaging cortical architecture and dynamics at high spatial and temporal resolution with new voltage-sensitive dyes. Neuron 24:1–12

    Article  Google Scholar 

  • Smith PH, Populin LC (2001) Fundamental differences between the thalamocortical recepient layers of the cat auditory and visual cortices. J Comp Neurol 13:381–398

    Google Scholar 

  • Van Essen DC, Anderson CH, Felleman DJ (1992) Information processing in the primate visual system—an integrated systems perspective. Science 255:419–423

    Article  PubMed  Google Scholar 

  • von Melchner L, Pallas SL, Sur M (2000) Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871–876

    Article  CAS  Google Scholar 

  • Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13–31

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by grants from the John Templeton Foundation and the Mind Science Foundation. We like to thank Dr. Andrew King for his input and Dr. Sue Totterdell for her help in histology.

Author information

Authors and Affiliations

  1. Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK

    Subhojit Chakraborty & Susan A. Greenfield

  2. Philosophy Faculty and Oxford Uehiro Centre for Practical Ethics, University of Oxford, Littlegate House, St Ebbes Street, Oxford, OX1 1PT, UK

    Anders Sandberg

  3. Neurophysiology, MRC Clinical Sciences Centre, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London, W12 0NN, UK

    Subhojit Chakraborty

Authors
  1. Subhojit Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anders Sandberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan A. Greenfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susan A. Greenfield.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chakraborty, S., Sandberg, A. & Greenfield, S.A. Differential dynamics of transient neuronal assemblies in visual compared to auditory cortex. Exp Brain Res 182, 491–498 (2007). https://doi.org/10.1007/s00221-007-1008-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-007-1008-y

Keywords

Search

Navigation