Journal of Comparative Physiology A

, Volume 197, Issue 1, pp 97–108

Interval-counting neurons in the anuran auditory midbrain: factors underlying diversity of interval tuning

  • Gary J. Rose
  • Christopher J. Leary
  • Christofer J. Edwards
Original Paper

Abstract

In anurans, the temporal patterning of sound pulses is the primary information used for differentiating between spectrally similar calls. One class of midbrain neurons, referred to as ‘interval-counting’ cells, appears to be particularly important for discriminating among calls that differ in pulse repetition rate (PRR). These cells only respond after several pulses are presented with appropriate interpulse intervals. Here we show that the range of selectivity and sharpness of interval tuning vary considerably across neurons. Whole-cell recordings revealed that neurons showing temporally summating excitatory postsynaptic potentials (EPSPs) with little or no inhibition or activity-dependent enhancement of excitation exhibited low-pass or band-pass tuning to slow PRRs. Neurons that showed inhibition and rate-dependent enhancement of excitation, however, were band-pass or high-pass to intermediate or fast PRRs. Surprisingly, across cells, interval tuning based on membrane depolarization and spike rate measures were not significantly correlated. Neurons that lacked inhibition showed the greatest disparities between these two measures of interval tuning. Cells that showed broad membrane potential-based tuning, for example, varied considerably in their spike rate-based tuning; narrow spike rate-based tuning resulted from ‘thresholding’ processes, whereby only the largest depolarizations triggered spikes. The potential constraints associated with generating interval tuning in this manner are discussed.

Keywords

Whole-cell Auditory Midbrain Temporal processing Amplitude modulation 

References

  1. Alder TB, Rose GJ (1998) Long-term temporal integration in the anuran auditory system. Nat Neurosci 1:519–522CrossRefPubMedGoogle Scholar
  2. Alder TB, Rose GJ (2000) Integration and recovery processes contribute to the temporal selectivity of neurons in the northern leopard frog, Rana pipiens. J Comp Physiol A 186:923–937CrossRefPubMedGoogle Scholar
  3. Aubie B, Becker S, Faure PA (2009) Computational models of millisecond level duration tuning in neural circuits. J Neurosci 29:9255–9270CrossRefPubMedGoogle Scholar
  4. Brenowitz EA, Rose GJ (1994) Behavioural plasticity mediates aggression in choruses of the Pacific treefrog. Anim Behav 47:633–641CrossRefGoogle Scholar
  5. Buonomano DV (2000) Decoding temporal information: a model based on short-term synaptic plasticity. J Neurosci 20:1129–1141PubMedGoogle Scholar
  6. Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20:479–484Google Scholar
  7. Carlson BA (2009) Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. J Neurosci 29:9417–9428CrossRefPubMedGoogle Scholar
  8. Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264:847–850CrossRefPubMedGoogle Scholar
  9. Casseday JH, Covey E, Grothe B (1997) Neural selectivity and tuning for sinusoidal frequency modulations in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:1595–1605PubMedGoogle Scholar
  10. Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New YorkGoogle Scholar
  11. Edwards CJ, Rose GJ (2003) Interval-integration underlies amplitude modulation band-suppression selectivity in the anuran midbrain. J Comp Physiol A 189:907–914CrossRefGoogle Scholar
  12. Edwards CJ, Alder TB, Rose GJ (2002) Auditory midbrain neurons that count. Nat Neurosci 5:934–936CrossRefPubMedGoogle Scholar
  13. Edwards CJ, Leary CJ, Rose GJ (2007) Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci 27:13384–13392CrossRefPubMedGoogle Scholar
  14. Edwards CJ, Leary CJ, Rose GJ (2008) Mechanisms of long-interval selectivity in midbrain auditory neurons: roles of excitation, inhibition, and plasticity. J Neurophysiol 100:3407–3416CrossRefPubMedGoogle Scholar
  15. Ehret G (1996) Common rules of communication sound perception. In: Kanwal JS, Ehret G (eds) Behavior and neurodynamics for auditory communication. Cambridge University Press, CambridgeGoogle Scholar
  16. Fortune ES, Rose GJ (2000) Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information. J Neurosci 20:7122–7130PubMedGoogle Scholar
  17. Geis HR, Borst JGG (2009) Intracellular responses of neurons in the mouse inferior colliculus to sinusoidal amplitude-modulated tones. J Neurophysiol 101:2002–2016CrossRefPubMedGoogle Scholar
  18. Gerhardt HC (1982) Sound pattern recognition in some North American treefrogs (Anura: Hylidae): implications for mate choice. Am Zool 22:581–595Google Scholar
  19. Gerhardt HC (1988) Acoustic properties used in call recognition by frogs and toads. In: Fritzch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New YorkGoogle Scholar
  20. Gerhardt HC (2001) Acoustic communication in two groups of closely related treefrogs. Adv Study Behav 30:99–167CrossRefGoogle Scholar
  21. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, Chicago, ILGoogle Scholar
  22. Gittelman JX, Na L, Pollak GD (2009) Mechanisms underlying directional selectivity for frequency-modulated sweeps in the inferior colliculus revealed by in vivo whole-cell recordings. J Neurosci 29:13030–13041CrossRefPubMedGoogle Scholar
  23. Grothe B (1994) Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. J Neurophysiol 71:706–721PubMedGoogle Scholar
  24. Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115–142CrossRefPubMedGoogle Scholar
  25. Large EW, Crawford JD (2002) Auditory temporal computation: interval selectivity based on post-inhibitory rebound. J Comput Neurosci 13:125–142CrossRefPubMedGoogle Scholar
  26. Leary CJ, Edwards CJ, Rose GJ (2008) Midbrain auditory neurons integrate excitation and inhibition to generate duration selectivity: an in-vivo whole-cell patch study in anurans. J Neurosci 28:5481–5493CrossRefPubMedGoogle Scholar
  27. Pluta SR, Kawasaki M (2010) Temporal selectivity in midbrain neurons identified by modal variation in active sensing. J Neurophysiol 104:498–507CrossRefPubMedGoogle Scholar
  28. Priebe NJ, Ferster D (2005) Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45:133–145CrossRefPubMedGoogle Scholar
  29. Rose GJ, Brenowitz EA (1997) Plasticity of aggressive thresholds in Hyla regilla: discrete accommodation to encounter calls. Anim Behav 53:353–361CrossRefGoogle Scholar
  30. Rose GJ, Brenowitz EA (2002) Pacific treefrogs use temporal integration to differentiate advertisement from encounter calls. Anim Behav 63:1183–1190CrossRefGoogle Scholar
  31. Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog Rana pipiens. Science 219:1087–1089CrossRefPubMedGoogle Scholar
  32. Rose GJ, Capranica RR (1984) Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters. J Comp Physiol A 154:211–219CrossRefGoogle Scholar
  33. Rose G, Capranica RR (1985) Sensitivity to amplitude modulated sounds in the anuran auditory nervous system. J Neurophysiol 53:446–465PubMedGoogle Scholar
  34. Rose GJ, Fortune ES (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26:89–94PubMedGoogle Scholar
  35. Rose GJ, Gooler DM (2007) Function of the anuran central auditory system. In: Feng AS, Narins PM, Fay RH, Popper AH (eds) Hearing and sound communication in amphibians. Springer handbook of auditory research. Springer-Verlag, New YorkGoogle Scholar
  36. Schwartz JJ, Huth K, Hunce R, Lentine B (2010) Effects of anomalous pulse timing on call discrimination by females of the gray treefrog (Hyla versicolor): behavioural correlates of neurobiology. J Exp Biol 213:2066–2072CrossRefPubMedGoogle Scholar
  37. Wells KD, Schwartz JJ (2007) The behavioral ecology of anuran communication. In: Feng AS, Narins PM, Fay RH, Popper AH (eds) Hearing and sound communication in amphibians. Springer handbook of auditory research. Springer-Verlag, New York, pp 44–86Google Scholar
  38. Zhang LI, Tan AYY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424:201–205CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Gary J. Rose
    • 1
  • Christopher J. Leary
    • 1
    • 2
  • Christofer J. Edwards
    • 1
  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA
  2. 2.Department of BiologyUniversity of MississippiOxfordUSA

Personalised recommendations