Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Auditory aversive learning increases discrimination thresholds

Abstract

Animal studies of discriminative fear conditioning traditionally use stimuli that are distant in physical features and thus easily distinguished perceptually. Independently, human studies have shown that training mostly improves discrimination thresholds. We found that aversive learning actually induced an increase in discrimination thresholds in humans and that subjective aversion during conditioning predicted the individual threshold change. This counterintuitive performance deterioration occurred when using odors or sounds as aversive reinforcers and was not a result of attentional distraction or decision bias. In contrast, positive reinforcement or mere exposure induced the typically reported decrease in thresholds. Our findings indicate that aversive outcomes induce wider stimulus generalization by modulating perceptual thresholds, suggesting the engagement of low-level mechanisms. We suggest that for risk- or loss-related stimuli, less specificity could be a benefit, as it invokes the same mechanisms that respond quickly and efficiently in the face of danger.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Aversive tone-odor conditioning increases discrimination thresholds.
Figure 2: Psychometric curves before and after aversive conditioning.
Figure 3: Individual implicit aversiveness predicts change in discrimination thresholds.
Figure 4: Aversive tones also cause increase in thresholds.
Figure 5: Discrimination thresholds persist after 24 h.
Figure 6: The potential contribution of distracted attention and decision bias to the change in discrimination thresholds.

Similar content being viewed by others

References

  1. LeDoux, J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184 (2000).

    Article  CAS  Google Scholar 

  2. Fanselow, M.S. & Poulos, A.M. The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 56, 207–234 (2005).

    Article  Google Scholar 

  3. Maren, S. & Quirk, G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5, 844–852 (2004).

    Article  CAS  Google Scholar 

  4. Armony, J.L., Servan-Schreiber, D., Romanski, L.M., Cohen, J.D. & LeDoux, J.E. Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats. Cereb. Cortex 7, 157–165 (1997).

    Article  CAS  Google Scholar 

  5. Chavez, C.M., McGaugh, J.L. & Weinberger, N.M. The basolateral amygdala modulates specific sensory memory representations in the cerebral cortex. Neurobiol. Learn. Mem. 91, 382–392 (2009).

    Article  Google Scholar 

  6. Laxmi, T.R., Stork, O. & Pape, H.C. Generalisation of conditioned fear and its behavioural expression in mice. Behav. Brain Res. 145, 89–98 (2003).

    Article  Google Scholar 

  7. Shaban, H. et al. Generalization of amygdala LTP and conditioned fear in the absence of presynaptic inhibition. Nat. Neurosci. 9, 1028–1035 (2006).

    Article  CAS  Google Scholar 

  8. Duvarci, S., Bauer, E.P. & Pare, D. The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J. Neurosci. 29, 10357–10361 (2009).

    Article  CAS  Google Scholar 

  9. Antunes, R. & Moita, M.A. Discriminative auditory fear learning requires both tuned and nontuned auditory pathways to the amygdala. J. Neurosci. 30, 9782–9787 (2010).

    Article  CAS  Google Scholar 

  10. Han, J.H. et al. Increasing CREB in the auditory thalamus enhances memory and generalization of auditory conditioned fear. Learn. Mem. 15, 443–453 (2008).

    Article  Google Scholar 

  11. Pearce, J.M. Animal Learning and Cognition: An Introduction (Psychology Press, 2008).

  12. Kurt, S. & Ehret, G. Auditory discrimination learning and knowledge transfer in mice depends on task difficulty. Proc. Natl. Acad. Sci. USA 107, 8481–8485 (2010).

    Article  CAS  Google Scholar 

  13. Weinberger, N.M. Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn. Mem. 14, 1–16 (2007).

    Article  Google Scholar 

  14. Li, W., Howard, J.D., Parrish, T.B. & Gottfried, J.A. Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319, 1842–1845 (2008).

    Article  CAS  Google Scholar 

  15. Schechtman, E., Laufer, O. & Paz, R. Negative valence widens generalization of learning. J. Neurosci. 30, 10460–10464 (2010).

    Article  CAS  Google Scholar 

  16. Fahle, M. & Poggio, T. eds. Perceptual Learning (MIT Press, 2002).

  17. Wright, B.A. & Zhang, Y. A review of the generalization of auditory learning. Phil. Trans. R. Soc. Lond. B 364, 301–311 (2009).

    Article  Google Scholar 

  18. Roelfsema, P.R., van Ooyen, A. & Watanabe, T. Perceptual learning rules based on reinforcers and attention. Trends Cogn. Sci. 14, 64–71 (2010).

    Article  Google Scholar 

  19. Ahissar, M., Nahum, M., Nelken, I. & Hochstein, S. Reverse hierarchies and sensory learning. Phil. Trans. R. Soc. Lond. B 364, 285–299 (2009).

    Article  Google Scholar 

  20. Gilbert, C.D. & Sigman, M. Brain states: top-down influences in sensory processing. Neuron 54, 677–696 (2007).

    Article  CAS  Google Scholar 

  21. Buonomano, D.V. & Merzenich, M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998).

    Article  CAS  Google Scholar 

  22. Weinberger, N.M. Specific long-term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 5, 279–290 (2004).

    Article  CAS  Google Scholar 

  23. Shepard, R.N. Toward a universal law of generalization for psychological science. Science 237, 1317–1323 (1987).

    Article  CAS  Google Scholar 

  24. McLaren, I.P. & Mackintosh, N.J. Associative learning and elemental representation: II. Generalization and discrimination. Anim. Learn. Behav. 30, 177–200 (2002).

    Article  CAS  Google Scholar 

  25. Livneh, U. & Paz, R. An implicit measure of olfactory performance for non-human primates reveals aversive and pleasant odor conditioning. J. Neurosci. Methods 192, 90–95 (2010).

    Article  Google Scholar 

  26. Amitay, S., Irwin, A. & Moore, D.R. Discrimination learning induced by training with identical stimuli. Nat. Neurosci. 9, 1446–1448 (2006).

    Article  CAS  Google Scholar 

  27. Watanabe, T., Nanez, J.E. & Sasaki, Y. Perceptual learning without perception. Nature 413, 844–848 (2001).

    Article  CAS  Google Scholar 

  28. Macmillan, N.A. & Creelman, C.D. Detection Theory: A User's Guide (Psychology Press, 2004).

  29. Wesson, D.W. & Wilson, D.A. Smelling sounds: olfactory-auditory sensory convergence in the olfactory tubercle. J. Neurosci. 30, 3013–3021 (2010).

    Article  CAS  Google Scholar 

  30. Davis, M. & Whalen, P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 6, 13–34 (2001).

    Article  CAS  Google Scholar 

  31. Bordi, F. & LeDoux, J.E. Response properties of single units in areas of rat auditory thalamus that project to the amygdala. I. Acoustic discharge patterns and frequency receptive fields. Exp. Brain Res. 98, 261–274 (1994).

    Article  CAS  Google Scholar 

  32. Quirk, G.J., Armony, J.L. & LeDoux, J.E. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19, 613–624 (1997).

    Article  CAS  Google Scholar 

  33. Dunsmoor, J.E., Prince, S.E., Murty, V.P., Kragel, P.A. & Labar, K.S. Neurobehavioral mechanisms of human fear generalization. Neuroimage 55, 1878–1888 (2011).

    Article  Google Scholar 

  34. Morris, J.S., Friston, K.J. & Dolan, R.J. Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proc. Biol. Sci. 265, 649–657 (1998).

    Article  CAS  Google Scholar 

  35. Polley, D.B., Heiser, M.A., Blake, D.T., Schreiner, C.E. & Merzenich, M.M. Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proc. Natl. Acad. Sci. USA 101, 16351–16356 (2004).

    Article  CAS  Google Scholar 

  36. Paz, R., Wise, S.P. & Vaadia, E. Viewing and doing: similar cortical mechanisms for perceptual and motor learning. Trends Neurosci. 27, 496–503 (2004).

    Article  CAS  Google Scholar 

  37. Ahissar, M. & Hochstein, S. Task difficulty and the specificity of perceptual learning. Nature 387, 401–406 (1997).

    Article  CAS  Google Scholar 

  38. Karni, A. & Sagi, D. The time course of learning a visual skill. Nature 365, 250–252 (1993).

    Article  CAS  Google Scholar 

  39. Bordi, F. & LeDoux, J. Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum. J. Neurosci. 12, 2493–2503 (1992).

    Article  CAS  Google Scholar 

  40. Haddad, R. et al. A metric for odorant comparison. Nat. Methods 5, 425–429 (2008).

    Article  CAS  Google Scholar 

  41. Polley, D.B., Steinberg, E.E. & Merzenich, M.M. Perceptual learning directs auditory cortical map reorganization through top-down influences. J. Neurosci. 26, 4970–4982 (2006).

    Article  CAS  Google Scholar 

  42. Yehuda, R. & LeDoux, J. Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56, 19–32 (2007).

    Article  CAS  Google Scholar 

  43. Lissek, S. et al. Overgeneralization of conditioned fear as a pathogenic marker of panic disorder. Am. J. Psychiatry 167, 47–55 (2010).

    Article  Google Scholar 

  44. Dunsmoor, J.E., Mitroff, S.R. & LaBar, K.S. Generalization of conditioned fear along a dimension of increasing fear intensity. Learn. Mem. 16, 460–469 (2009).

    Article  Google Scholar 

  45. Levitt, H. Transformed up-down methods in psychoacoustics. J. Acoust. Soc. Am. 49 (suppl. 2), 467–477 (1971).

    Article  Google Scholar 

  46. Hawkey, D.J., Amitay, S. & Moore, D.R. Early and rapid perceptual learning. Nat. Neurosci. 7, 1055–1056 (2004).

    Article  CAS  Google Scholar 

  47. Johnson, B.N. & Sobel, N. Methods for building an olfactometer with known concentration outcomes. J. Neurosci. Methods 160, 231–245 (2007).

    Article  Google Scholar 

  48. Yeshurun, Y., Dudai, Y. & Sobel, N. Working memory across nostrils. Behav. Neurosci. 122, 1031–1037 (2008).

    Article  Google Scholar 

  49. Neumann, D.L. & Waters, A.M. The use of an unpleasant sound as an unconditional stimulus in a human aversive Pavlovian conditioning procedure. Biol. Psychol. 73, 175–185 (2006).

    Article  Google Scholar 

  50. Marcell, M.M., Borella, D., Greene, M., Kerr, E. & Rogers, S. Confrontation naming of environmental sounds. J. Clin. Exp. Neuropsychol. 22, 830–864 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Sagi for discussions. This work was supported by a Minerva Foundation and an Israel Science Foundation Grant to R.P., an Alon and Marie-Curie Fellow.

Author information

Authors and Affiliations

Authors

Contributions

R.P. conceived the hypothesis. R.P., N.S. and J.R. designed experiments. J.R. performed the experiments. R.P. and J.R. performed the data analyses and wrote the manuscript.

Corresponding author

Correspondence to Rony Paz.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Resnik, J., Sobel, N. & Paz, R. Auditory aversive learning increases discrimination thresholds. Nat Neurosci 14, 791–796 (2011). https://doi.org/10.1038/nn.2802

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2802

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing