Skip to main content

Advertisement

Log in

Encoding Stimulus Information by Spike Numbers and Mean Response Time in Primary Auditory Cortex

Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Neurons can transmit information about sensory stimuli via their firing rate, spike latency, or by the occurrence of complex spike patterns. Identifying which aspects of the neural responses actually encode sensory information remains a fundamental question in neuroscience. Here we compared various approaches for estimating the information transmitted by neurons in auditory cortex in two very different experimental paradigms, one measuring spatial tuning and the other responses to complex natural stimuli. We demonstrate that, in both cases, spike counts and mean response times jointly carry essentially all the available information about the stimuli. Thus, in auditory cortex, whereas spike counts carry only partial information about stimulus identity or location, the additional availability of relatively coarse temporal information is sufficient in order to extract essentially all the sensory information available in the spike discharge pattern, at least for the relatively short stimuli (< ∼ 100 ms) commonly used in auditory research.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

References

  • Bar-Yosef O, Rotman Y, Nelken I (2002) Responses of neurons in cat primary auditory cortex to bird chirps: Effects of temporal and spectral context. J. Neurosci. 22: 8619–8632.

    PubMed  Google Scholar 

  • Bialek W, Rieke F, de Ruyter van Steveninck RR, Warland D (1991) Reading a neural code. Science 252: 1854–1857.

    PubMed  Google Scholar 

  • Brugge JF, Reale RA, Hind JE (1996) The structure of spatial receptive fields of neurons in primary auditory cortex of the cat. J. Neurosci. 16: 4420–4437.

    PubMed  Google Scholar 

  • Brugge JF, Reale RA, Jenison RL, Schnupp J (2001) Auditory cortical spatial receptive fields. Audiol Neurootol. 6: 173–177.

    Article  PubMed  Google Scholar 

  • Cover T, Thomas J (1991) Elements of Information Theory. Wiley and Sons, NY.

    Google Scholar 

  • DeGroot MH, Schervish MJ (2001) Probability and Statistics. Addison-Wesley, Boston, MA.

    Google Scholar 

  • Duda RO, Hart PE, Stork DG (2000) Pattern Classification, 2nd edition. John Wiley and Sons.

  • Furukawa S, Middlebrooks JC (2002) Cortical representation of auditory space: Information-bearing features of spike patterns. J. Neurophysiol. 87: 1749–1762.

    PubMed  Google Scholar 

  • Jenison RL, Reale RA (2003) Likelihood approaches to sensory coding in auditory cortex. Network 14: 83–102.

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Machens CK, Schutze H, Franz A, Kolesnikova O, Stemmler MB, Ronacher B, Herz AV (2003) Single auditory neurons rapidly discriminate conspecific communication signals. Nat Neurosci. 6: 341–342.

    Article  PubMed  Google Scholar 

  • Middlebrooks JC, Clock AE, Xu L, Green DM (1994) A panoramic code for sound location by cortical neurons. Science 264: 842–844.

    PubMed  Google Scholar 

  • Middlebrooks JC, Xu L, Eddins AC, Green DM (1998) Codes for sound-source location in nontonotopic auditory cortex. J. Neurophysiol. 80: 863–881.

    PubMed  Google Scholar 

  • Mrsic-Flogel TD, King AJ, Schnupp JWH (2005) Encoding of virtual acoustic space stimuli by neurons in ferret primary auditory cortex. J. Neurophys. 93: 3489–3503.

    Article  Google Scholar 

  • Paninski L (2003) Estimation of entropy and mutual information. Neural. Comput. 15: 1191–1253.

    Article  Google Scholar 

  • Panzeri S, Treves A (1996) Analytical estimates of limited sampling biases in different information measures. Network 7: 87–101.

    Google Scholar 

  • Panzeri S, Schultz SR (2001) A unified approach to the study of temporal, correlational, and rate coding. Neural Comput. 13: 1311–1349.

    Article  PubMed  Google Scholar 

  • Panzeri S, Schultz SR, Treves A, Rolls ET (1999a) Correlations and the encoding of information in the nervous system. Proc. R. Soc. Lond B. Biol. Sci. 266: 1001–1012.

    Article  Google Scholar 

  • Panzeri S, Treves A, Schultz S, Rolls ET (1999b) On decoding the responses of a population of neurons from short time windows. Neural Comput. 11: 1553–1577.

    Article  Google Scholar 

  • Panzeri S, Petroni F, Petersen RS, Diamond ME (2003) Decoding neuronal population activity in rat somatosensory cortex: Role of columnar organization. Cereb. Cortex 13: 45–52.

    Article  PubMed  Google Scholar 

  • Panzeri S, Petersen RS, Schultz SR, Lebedev M, Diamond ME (2001) The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29: 769–777.

    Article  PubMed  Google Scholar 

  • Petersen RS, Panzeri S, Diamond ME (2001) Population coding of stimulus location in rat somatosensory cortex. Neuron 32: 503–514.

    Article  PubMed  Google Scholar 

  • Petersen RS, Panzeri S, Diamond ME (2002) The role of individual spikes and spike patterns in population coding of stimulus location in rat somatosensory cortex. Biosystems 67: 187–193.

    Article  PubMed  Google Scholar 

  • Pola G, Thiele A, Hoffmann KP, Panzeri S (2003) An exact method to quantify the information transmitted by different mechanisms of correlational coding. Network 14: 35–60.

    PubMed  Google Scholar 

  • Reale RA, Jenison RL, Brugge JF (2003) Directional sensitivity of neurons in the primary auditory (AI) cortex: Effects of sound-source intensity level. J. Neurophysiol. 89: 1024–1038.

    PubMed  Google Scholar 

  • Reich DS, Mechler F, Victor JD (2001) Formal and attribute-specific information in primary visual cortex. J. Neurophysiol. 85: 305–318.

    PubMed  Google Scholar 

  • Rieke F, Warland D, deRuyter van Steveninck R, Bialek W (1997) Spikes. MIT Press, Cambridge, MA.

    Google Scholar 

  • Rolls ET, Treves A, Tovee MJ (1997) The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex. Exp. Brain Res. 114: 149–162.

    PubMed  Google Scholar 

  • Rotman Y, Bar-Yosef O, Nelken I (2001) Relating cluster and population responses to natural sounds and tonal stimuli in cat primary auditory cortex. Hear Res. 152: 110–127.

    Article  PubMed  Google Scholar 

  • Schervish MJ (1995) Theory of Statistics. Springer, New York.

    Google Scholar 

  • Schnupp JWH, Mrsic-Flogel TD, King AJ (2001) Linear processing of spatial cues in primary auditory cortex. Nature 414: 200– 204.

    Article  PubMed  Google Scholar 

  • Slonim N, Tishby N (2000) Agglomerative Information Bottleneck. In: (SA Solla, TK Leen, KR Muller, eds), Advances in Neural Information Processing Systems 12. MIT Press, Cambridge, MA.

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edition. W.H. Freeman, New York.

    Google Scholar 

  • Treves A (2001) Information Coding in Higher Sensory and Memory Areas. In: F Moss, S Gielen, eds., Handbook of Biological Physics, Vol. 4: Neuro-Informatics and Neural Modelling. Elsevier, Amsterdam, pp. 825–852.

  • Treves A, Panzeri S (1995) The upward bias in measures of information derived from limited data samples. Neural Computation 7: 399–407.

    Google Scholar 

  • Van Rullen R, Thorpe SJ (2001) Rate coding versus temporal order coding: What the retinal ganglion cells tell the visual cortex. Neural Comput. 13: 1255–1283.

    Article  PubMed  Google Scholar 

  • Van Rullen R, Thorpe SJ (2002) Surfing a spike wave down the ventral stream. Vision Res. 42: 2593–2615.

    Article  PubMed  Google Scholar 

  • Van Rullen R, Gautrais J, Delorme A, Thorpe S (1998) Face processing using one spike per neurone. Biosystems 48: 229–239.

    Article  PubMed  Google Scholar 

  • Victor JD (2000) Asymptotic bias in information estimates and the exponential (Bell) polynomials. Neural Comput. 12: 2797–2804.

    Article  PubMed  Google Scholar 

  • Victor JD (2002) Binless strategies for estimation of information from neural data. Phys. Rev. E 66: 51903.

    Google Scholar 

  • Victor JD, Purpura KP (1996) Nature and precision of temporal coding in visual cortex: A metric-space analysis. J. Neurophys. 76: 1310–1326.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Israel Nelken.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nelken, I., Chechik, G., Mrsic-Flogel, T.D. et al. Encoding Stimulus Information by Spike Numbers and Mean Response Time in Primary Auditory Cortex. J Comput Neurosci 19, 199–221 (2005). https://doi.org/10.1007/s10827-005-1739-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-005-1739-3

Keywords

Navigation