Abstract
The ability to detect rare auditory events can be critical for survival. We report here that neurons in cat primary auditory cortex (A1) responded more strongly to a rarely presented sound than to the same sound when it was common. For the rare stimuli, we used both frequency and amplitude deviants. Moreover, some A1 neurons showed hyperacuity for frequency deviants—a frequency resolution one order of magnitude better than receptive field widths in A1. In contrast, auditory thalamic neurons were insensitive to the probability of frequency deviants. These phenomena resulted from stimulus-specific adaptation in A1, which may be a single-neuron correlate of an extensively studied cortical potential—mismatch negativity—that is evoked by rare sounds. Our results thus indicate that A1 neurons, in addition to processing the acoustic features of sounds, may also be involved in sensory memory and novelty detection.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Ohzawa, I., Sclar, G. & Freeman, R.D. Contrast gain control in the cat visual cortex. Nature 298, 266–268 (1982).
Müller, J.R., Metha, A.B., Krauskopf, J. & Lennie, P. Rapid adaptation in visual cortex to the structure of images. Science 285, 1405–1408 (1999).
Fairhall, A.L., Lewen, G.D., Bialek, W. & de Ruyter Van Steveninck, R.R. Efficiency and ambiguity in an adaptive neural code. Nature 412, 787–792 (2001).
Movshon, J.A. & Lennie, P. Pattern-selective adaptation in visual cortical neurones. Nature 278, 850–852 (1979).
Saul, A.B. & Cynader, M.S. Adaptation in single units in visual cortex: the tuning of aftereffects in the spatial domain. Vis. Neurosci. 2, 593–607 (1989).
Dragoi, V., Sharma, J. & Sur, M. Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28, 287–298 (2000).
Dragoi, V., Rivadulla, C. & Sur, M. Foci of orientation plasticity in visual cortex. Nature 411, 80–86 (2001).
Condon, C.D. & Weinberger, N.M. Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. Behav. Neurosci. 105, 416–430 (1991).
Malone, B.J. & Semple, M.N. Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus. J. Neurophysiol. 86, 1113–1130 (2001).
Malone, B.J., Scott, B.H. & Semple, M.N. Context-dependent adaptive coding of interaural phase disparity in the auditory cortex of awake macaques. J. Neurosci. 22, 4625–4638 (2002).
Sanes, D.H., Malone, B.J. & Semple, M.N. Role of synaptic inhibition in processing of dynamic binaural level stimuli. J. Neurosci. 18, 794–803 (1998).
Nelken, I., Rotman, Y. & Bar-Yosef, O. Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397, 154–157 (1999).
Näätänen, R. Attention and Brain Function (Lawrence Erlbaum, Hillsdale, New Jersey, 1992).
Tiitinen, H., May, P., Reinikainen, K. & Näätänen, R. Attentive novelty detection in humans is governed by pre-attentive sensory memory. Nature 372, 90–92 (1994).
Picton, T.W., Alain, C., Otten, L., Ritter, W. & Achim, A. Mismatch negativity: different water in the same river. Audiol. Neurootol. 5, 111–139 (2000).
Jacobsen, T. & Schröger, E. Is there pre-attentive memory-based comparison of pitch? Psychophysiology 38, 723–727 (2001).
Näätänen, R., Tervaniemi, M., Sussman, E., Paavilainen, P. & Winkler, I. “Primitive intelligence” in the auditory cortex. Trends Neurosci. 24, 283–288 (2001).
Csépe, V., Karmos, G. & Molnár, M. Evoked potential correlates of stimulus deviance during wakefulness and sleep in cat—animal model of mismatch negativity. Electroencephalogr. Clin. Neurophysiol. 66, 571–578 (1987).
Csépe, V., Molnár, M., Karmos, G. & Winkler, I. Effect of changes in stimulus frequency on auditory evoked potentials in awake and anaesthetized cats. in Sleep 88 (eds. Horne, J. & Lovie, P.) 210–211 (Gustav Fischer, Stuttgart/New York, 1989).
Pincze, Z., Lakatos, P., Rajkai, C., Ulbert, I. & Karmos, G. Separation of mismatch negativity and the N1 wave in the auditory cortex of the cat: a topographic study. Clin. Neurophysiol. 112, 778–784 (2001).
Javitt, D.C., Steinschneider, M., Schroeder, C.E., Vaughan, H.G. Jr. & Arezzo, J.C. Detection of stimulus deviance within primate primary auditory cortex: intracortical mechanisms of mismatch negativity (MMN) generation. Brain Res. 667, 192–200 (1994).
May, P. et al. Frequency change detection in human auditory cortex. J. Comput. Neurosci. 6, 99–120 (1999).
Fischer, C., Morlet, D. & Giard, M. Mismatch negativity and N100 in comatose patients. Audiol. Neurootol. 5, 192–197 (2000).
Javitt, D.C. Intracortical mechanisms of mismatch negativity dysfunction in schizophrenia. Audiol. Neurootol. 5, 207–215 (2000).
Kujala, T. & Näätänen, R. The mismatch negativity in evaluating central auditory dysfunction in dyslexia. Neurosci. Biobehav. Rev. 25, 535–543 (2001).
Deouell, L.Y., Hamalainen, H. & Bentin, S. Unilateral neglect after right-hemisphere damage: contributions from event-related potentials. Audiol. Neurootol. 5, 225–234 (2000).
Kraus, N. et al. Discrimination of speech-like contrasts in the auditory thalamus and cortex. J. Acoust. Soc. Am. 96, 2758–2768 (1994).
King, C., McGee, T., Rubel, E.W., Nicol, T. & Kraus, N. Acoustic features and acoustic changes are represented by different central pathways. Hear. Res. 85, 45–52 (1995).
Kraus, N., McGee, T., Littman, T., Nicol, T. & King, C. Nonprimary auditory thalamic representation of acoustic change. J. Neurophysiol. 72, 1270–1277 (1994).
Andersen, R.A., Knight, P.L. & Merzenich, M.M. The thalamocortical and corticothalamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: evidence for two largely segregated systems of connections. J. Comp. Neurol. 194, 663–701 (1980).
Markram, H., Wang, Y. & Tsodyks, M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc. Natl. Acad. Sci. USA 95, 5323–5328 (1998).
Phillips, D.P., Mendelson, J.R., Cynader, M.S. & Douglas, R.M. Responses of single neurones in cat auditory cortex to time-varying stimuli: frequency-modulated tones of narrow excursion. Exp. Brain. Res. 58, 443–454 (1985).
Calford, M.B. & Semple, M.N. Monaural inhibition in cat auditory cortex. J. Neurophysiol. 73, 1876–1891 (1995).
Brosch, M. & Schreiner, C.E. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77, 923–943 (1997).
Liberman, M.C. Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 63, 442–455 (1978).
Moore, B.C.J. Frequency analysis and pitch perception. in Human Psychophysics (eds. Yost, W.A., Popper, A.N. & Fay, R.R.) 56–115 (Springer, New York, 1993).
Delgutte, B. Physiological models for basic auditory percepts. in Auditory Computation (eds. Hawkins, H.L., McMullen, T.A., Popper, A.N. & Fay, R.R.) 157–220 (Springer, New York, 1996).
Amitay, S., Ahissar, M. & Nelken, I. Auditory processing deficits in reading disabled adults. J. Assoc. Res. Otolaryngol. 3, 302–320 (2002).
Ahissar, M., Protopapas, A., Reid, M. & Merzenich, M.M. Auditory processing parallels reading abilities in adults. Proc. Natl. Acad. Sci. USA 97, 6832–6837 (2000).
Masterton, R.B., Granger, E.M. & Glendenning, K.K. Psychoacoustical contribution of each lateral lemniscus. Hear. Res. 63, 57–70 (1992).
Bar-Yosef, O., Rotman, Y. & Nelken, I. Responses of neurons in cat primary auditory cortex to bird chirps: effects of temporal and spectral context. J. Neurosci. 22, 8619–8632 (2002).
Green, D.M. & Swets, J.A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).
Acknowledgements
We thank G. Morris and G. Chechik for critical reading of the manuscript, and G. Karmos, I. Winkler, L. Deouell, H. Pratt, S. Bentin, S. Marom and M. Ahissar for stimulating discussions on the SSA–MMN comparison. This work was supported by a Human Frontiers Science Program grant to I.N. and a Horowitz Foundation predoctoral fellowship to N.U.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Ulanovsky, N., Las, L. & Nelken, I. Processing of low-probability sounds by cortical neurons. Nat Neurosci 6, 391–398 (2003). https://doi.org/10.1038/nn1032
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1032
This article is cited by
-
Omission responses in local field potentials in rat auditory cortex
BMC Biology (2023)
-
Novelty detection in an auditory oddball task on freely moving rats
Communications Biology (2023)
-
A power law describes the magnitude of adaptation in neural populations of primary visual cortex
Nature Communications (2023)
-
Expectation violations enhance neuronal encoding of sensory information in mouse primary visual cortex
Nature Communications (2023)
-
Long- and short-term history effects in a spiking network model of statistical learning
Scientific Reports (2023)