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The Journal of Neuroscience, April 12, 2006, 26(15):3889-3898; doi:10.1523/JNEUROSCI.4986-05.2006

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Behavioral/Systems/Cognitive
Spike-Timing Codes Enhance the Representation of Multiple Simultaneous Sound-Localization Cues in the Inferior Colliculus

Steven M. Chase and Eric D. Young

Center for Hearing Sciences and Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21205

Correspondence should be addressed to Dr. Eric D. Young, 505 Traylor Research Building, 720 Rutland Avenue, Baltimore, MD 21205. Email: eyoung{at}bme.jhu.edu

To preserve multiple streams of independent information that converge onto a neuron, the information must be re-represented more efficiently in the neural response. Here we analyze the increase in the representational capacity of spike timing over rate codes using sound localization cues as an example.

The inferior colliculus receives convergent input from multiple auditory brainstem nuclei, including sound localization information such as interaural level differences (ILDs), interaural timing differences (ITDs), and spectral cues. Virtual space techniques were used to create stimulus sets varying in two sound-localization parameters each. Information about the cues was quantified using a spike distance metric that allows one to separate contributions to the information arising from spike rate and spike timing.

Spike timing enhances the representation of spectral and ILD cues at timescales averaging 12 ms. ITD information, however, is carried by a rate code. Comparing responses to frozen and random noise shows that the temporal information is mainly attributable to phase locking to temporal stimulus features, with an additional first-spike latency component. With rate-based codes, there is significant confounding of information about two cues presented simultaneously, meaning that the cues cannot be decoded independently. Spike-timing-based codes reduce this confounded information. Furthermore, the relative representation of the cues often changes as a function of the time resolution of the code, implying that information about multiple cues can be multiplexed onto individual spike trains.

Key words: information theory; inferior colliculus; sound localization; spectral notch; ILD; ITD; spike distance metrics

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Received Nov. 22, 2005; revised Feb. 17, 2006; accepted Feb. 18, 2006.

Correspondence should be addressed to Dr. Eric D. Young, 505 Traylor Research Building, 720 Rutland Avenue, Baltimore, MD 21205. Email: eyoung{at}bme.jhu.edu

This article has been cited by other articles:

				S. M. Chase and E. D. Young Cues for Sound Localization Are Encoded in Multiple Aspects of Spike Trains in the Inferior Colliculus J Neurophysiol, April 1, 2008; 99(4): 1672 - 1682. [Abstract] [Full Text] [PDF]

				M. Ter-Mikaelian, D. H. Sanes, and M. N. Semple Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil J. Neurosci., June 6, 2007; 27(23): 6091 - 6102. [Abstract] [Full Text] [PDF]

				G. B. Christianson and J. L. Pena Preservation of Spectrotemporal Tuning Between the Nucleus Laminaris and the Inferior Colliculus of the Barn Owl J Neurophysiol, May 1, 2007; 97(5): 3544 - 3553. [Abstract] [Full Text] [PDF]

				S. M. Chase and E. D. Young First-spike latency information in single neurons increases when referenced to population onset PNAS, March 20, 2007; 104(12): 5175 - 5180. [Abstract] [Full Text] [PDF]

				M. M. Van Wanrooij and A. J. Van Opstal Sound Localization Under Perturbed Binaural Hearing J Neurophysiol, January 1, 2007; 97(1): 715 - 726. [Abstract] [Full Text] [PDF]

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