Abstract
Neuronal activity patterns contain information in their temporal structure, indicating that information transfer between neurons may be optimized by temporal filtering. In the zebrafish olfactory bulb, subsets of output neurons (mitral cells) engage in synchronized oscillations during odour responses, but information about odour identity is contained mostly in non-oscillatory firing rate patterns. Using optogenetic manipulations and odour stimulation, we found that firing rate responses of neurons in the posterior zone of the dorsal telencephalon (Dp), a target area homologous to olfactory cortex, were largely insensitive to oscillatory synchrony of mitral cells because passive membrane properties and synaptic currents act as low-pass filters. Nevertheless, synchrony influenced spike timing. Moreover, Dp neurons responded primarily during the decorrelated steady state of mitral cell activity patterns. Temporal filtering therefore tunes Dp neurons to components of mitral cell activity patterns that are particularly informative about precise odour identity. These results demonstrate how temporal filtering can extract specific information from multiplexed neuronal codes.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Gerstner, W., Kreiter, A. K., Markram, H. & Herz, A. V. Neural codes: firing rates and beyond. Proc. Natl Acad. Sci. USA 94, 12740–12741 (1997)
Hutcheon, B. & Yarom, Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216–222 (2000)
Fries, P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32, 209–224 (2009)
Gütig, R. & Sompolinsky, H. The tempotron: a neuron that learns spike timing-based decisions. Nature Neurosci. 9, 420–428 (2006)
Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nature Rev. Neurosci. 3, 884–895 (2002)
Rabinovich, M., Huerta, R. & Laurent, G. Transient dynamics for neural processing. Science 321, 48–50 (2008)
Buzsaki, G. & Draguhn, A. Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004)
Singer, W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49–65 (1999)
Perez-Orive, J., Bazhenov, M. & Laurent, G. Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. J. Neurosci. 24, 6037–6047 (2004)
Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359–365 (2002)
Azouz, R. & Gray, C. M. Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo . Neuron 37, 513–523 (2003)
Bruno, R. M. & Sakmann, B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622–1627 (2006)
Gawne, T. J., Kjaer, T. W. & Richmond, B. J. Latency: another potential code for feature binding in striate cortex. J. Neurophysiol. 76, 1356–1360 (1996)
Hopfield, J. J. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33–36 (1995)
Gollisch, T. & Meister, M. Rapid neural coding in the retina with relative spike latencies. Science 319, 1108–1111 (2008)
Junek, S., Kludt, E., Wolf, F. & Schild, D. Olfactory Coding with Patterns of Response Latencies. Neuron 67, 872–884 (2010)
Spors, H., Wachowiak, M., Cohen, L. B. & Friedrich, R. W. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J. Neurosci. 26, 1247–1259 (2006)
Bathellier, B., Buhl, D. L., Accolla, R. & Carleton, A. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57, 586–598 (2008)
Cury, K. M. & Uchida, N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570–585 (2010)
Maass, W., Natschlager, T. & Markram, H. Real-time computing without stable states: a new framework for neural computation based on perturbations. Neural Comput. 14, 2531–2560 (2002)
Sugase, Y., Yamane, S., Ueno, S. & Kawano, K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 869–873 (1999)
Friedrich, R. W. & Laurent, G. Dynamic optimization of odor representations in the olfactory bulb by slow temporal patterning of mitral cell activity. Science 291, 889–894 (2001)
Ringach, D. L., Hawken, M. J. & Shapley, R. Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281–284 (1997)
Friedrich, R. W., Habermann, C. J. & Laurent, G. Multiplexing using synchrony in the zebrafish olfactory bulb. Nature Neurosci. 7, 862–871 (2004)
Mazor, O. & Laurent, G. Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661–673 (2005)
Yaksi, E., von Saint Paul, F., Niessing, J., Bundschuh, S. T. & Friedrich, R. W. Transformation of odor representations in target areas of the olfactory bulb. Nature Neurosci. 12, 474–482 (2009)
Miyamichi, K. et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191–196 (2011)
Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl Acad. Sci. USA 100, 13940–13945 (2003)
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neurosci. 8, 1263–1268 (2005)
Zhu, P. et al. Optogenetic dissection of neuronal circuits in zebrafish using viral gene transfer and the Tet system. Front. Neural Circuits 3, 21 (2009)
Laurent, G. & Naraghi, M. Odorant-induced oscillations in the mushroom bodies of the locust. J. Neurosci. 14, 2993–3004 (1994)
Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159–1163 (2001)
Franks, K. M. & Isaacson, J. S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49, 357–363 (2006)
Luna, V. M. & Schoppa, N. E. GABAergic circuits control input-spike coupling in the piriform cortex. J. Neurosci. 28, 8851–8859 (2008)
Ketchum, K. L. & Haberly, L. B. Synaptic events that generate fast oscillations in piriform cortex. J. Neurosci. 13, 3980–3985 (1993)
Yaksi, E. & Friedrich, R. W. Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nature Methods 3, 377–383 (2006)
Friedrich, R. W. & Korsching, S. I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18, 737–752 (1997)
Niessing, J. & Friedrich, R. W. Olfactory pattern classification by discrete neuronal network states. Nature 465, 47–52 (2010)
Stokes, C. C. & Isaacson, J. S. From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 67, 452–465 (2010)
Poo, C. & Isaacson, J. S. Odor representations in olfactory cortex: “sparse” coding, global inhibition, and oscillations. Neuron 62, 850–861 (2009)
Stopfer, M., Jayaraman, V. & Laurent, G. Intensity versus identity coding in an olfactory system. Neuron 39, 991–1004 (2003)
Jortner, R. A., Farivar, S. S. & Laurent, G. A simple connectivity scheme for sparse coding in an olfactory system. J. Neurosci. 27, 1659–1669 (2007)
Spence, R., Gerlach, G., Lawrence, C. & Smith, C. The behaviour and ecology of the zebrafish, Danio rerio . Biol. Rev. Camb. Philos. Soc. 83, 13–34 (2008)
Engeszer, R. E., Patterson, L. B., Rao, A. A. & Parichy, D. M. Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4, 21–40 (2007)
Sato, Y., Miyasaka, N. & Yoshihara, Y. Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. J. Neurosci. 25, 4889–4897 (2005)
Higashijima, S., Masino, M. A., Mandel, G. & Fetcho, J. R. Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J. Neurophysiol. 90, 3986–3997 (2003)
Gossen, M. & Bujard, H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA 89, 5547–5551 (1992)
Miyasaka, N. et al. From the olfactory bulb to higher brain centers: genetic visualization of secondary olfactory pathways in zebrafish. J. Neurosci. 29, 4756–4767 (2009)
Mathieson, W. B. & Maler, L. Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J. Comp. Physiol. A 163, 489–506 (1988)
Pologruto, T. A., Sabatini, B. L. & Svoboda, K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003)
Suter, B. A. et al. Ephus: multipurpose data acquisition software for neuroscience experiments. Front. Neural Circuits 4, 100 (2010)
Tabor, R. & Friedrich, R. W. Pharmacological analysis of ionotropic glutamate receptor function in neuronal circuits of the zebrafish olfactory bulb. PLoS ONE 3, e1416 (2008)
Bhandawat, V., Olsen, S. R., Gouwens, N. W., Schlief, M. L. & Wilson, R. I. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nature Neurosci. 10, 1474–1482 (2007)
Acknowledgements
This work was supported by the Novartis Research Foundation, the Max-Planck-Society, the Swiss National Fonds (SNF), the Deutsche Forschungsgemeinschaft (DFG), the Human Frontier Science Program (HFSP), and the Whitaker Foundation (J.S.). We are grateful to S.-i. Higashijima for vglut2a-GFP transgenic fish and thank T. Frank, A. Lüthi, I. Namekawa and T. Oertner for comments on the manuscript.
Author information
Authors and Affiliations
Contributions
F.B. performed electrophysiological experiments, analysed data and wrote part of the manuscript. P.Z. generated transgenic fish, participated in the construction of the DMD device, performed optogenetic experiments, recorded LFPs and analysed data. J.S. constructed the DMD device and performed optogenetic experiments. Y.-P.Z.S. performed electrophysiological experiments, participated in the construction of the DMD device, performed calcium imaging experiments, recorded LFPs and analysed data. E.Y. participated in calcium imaging experiments. K.D. contributed channelrhodopsin-2 constructs. R.W.F. conceived the study, designed equipment, analysed data, performed modelling and wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-15 with legends and additional references. (PDF 2879 kb)
Supplementary Movie 1
This movie shows an example of an optical stimulus pattern with no synchronization (S = 0), slowed down in time. (AVI 4852 kb)
Supplementary Movie 2
Example of an optical stimulus pattern with high synchronization (S = 10; same spatial pattern as Supplementary Movie 1), slowed down in time. (AVI 4832 kb)
Rights and permissions
About this article
Cite this article
Blumhagen, F., Zhu, P., Shum, J. et al. Neuronal filtering of multiplexed odour representations. Nature 479, 493–498 (2011). https://doi.org/10.1038/nature10633
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature10633
This article is cited by
-
All-optical manipulation of the Drosophila olfactory system
Scientific Reports (2022)
-
A database and deep learning toolbox for noise-optimized, generalized spike inference from calcium imaging
Nature Neuroscience (2021)
-
A two-compartment model of synaptic computation and plasticity
Molecular Brain (2020)
-
Associative conditioning remaps odor representations and modifies inhibition in a higher olfactory brain area
Nature Neuroscience (2019)
-
Optogenetic stimulation of complex spatio-temporal activity patterns by acousto-optic light steering probes cerebellar granular layer integrative properties
Scientific Reports (2018)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.