Limited Segregation of Different Types of Sound Localization Information among Classes of Units in the Inferior Colliculus

Chase, Steven M.; Young, Eric D.

doi:10.1523/jneurosci.0915-05.2005

Cited by 65 publications

(45 citation statements)

References 61 publications

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“…1C. On average, the first-spike latency variation contains 0.70 Ϯ 0.41 (SD) bits of information about the stimuli, somewhat less than the information in spike count or ongoing spike timing (17,18).…”

Section: Resultsmentioning

confidence: 99%

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First-spike latency information in single neurons increases when referenced to population onset

Chase

Young

2007

Proc. Natl. Acad. Sci. U.S.A.

168

147

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It is well known that many stimulus parameters, such as sound location in the auditory system or contrast in the visual system, can modulate the timing of the first spike in sensory neurons. Could first-spike latency be a candidate neural code? Most studies measuring first-spike latency information assume that the brain has an independent reference for stimulus onset from which to extract latency. This assumption creates an obvious confound that casts doubt on the feasibility of first-spike latency codes. If latency is measured relative to an internal reference of stimulus onset calculated from the responses of the neural population, the information conveyed by the latency of single neurons might decrease because of correlated changes in latency across the population. Here we assess the effects of a realistic model of stimulus onset detection on the first-spike latency information conveyed by single neurons in the auditory system. Contrary to expectation, we find that on average, the information contained in single neurons does not decrease; in fact, the majority of neurons show a slight increase in the information conveyed by latency referenced to a population onset. Our results show that first-spike latency codes are a feasible mechanism for information transfer even when biologically plausible estimates of stimulus onset are taken into account.coding ͉ inferior colliculus ͉ mutual information ͉ sound localization T he first-spike latency has been shown to carry information in several sensory modalities, including the auditory (1, 2), visual (3, 4), and somatosensory (5-7) systems. However, most studies quantifying first-spike latency information assume that the brain has an independent reference for stimulus onset from which to extract latency. In the majority of situations, this independent onset reference does not exist; the need for a timing reference has caused some to question the ultimate feasibility of first-spike latency codes (8).A number of authors have suggested possible alternative latency measures (1,3,5,6), but few have actually compared the information contained in different onset references. Stecker and Middlebrooks (9) computed the information contained in the relative spike timing of pairs of simultaneously recorded neurons in auditory cortex, and Furukawa et al. (10) compared the median errors from neural-network estimates of location with similar data. In both cases, performance with relative-latency measures was worse than with an independent onset reference, presumably because using a single neuron as the onset reference increases the overall measurement jitter. Other authors (11-13) have investigated rank order codes, where information is conveyed by the relative order in which neurons fire. Jenison (14) has shown by using modeling and maximum likelihood techniques that correlation can, in principle, increase the information available in first-spike latency, provided the decoder knows the correlation structure. However, such location estimates get noisier when stimulus onset is estimate...

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Section: Resultsmentioning

confidence: 99%

“…The rationale for the design of these experiments is explained elsewhere (17,18). Two sets of 25 stimuli were used, varying in two binaural sound localization cues each.…”

Section: Resultsmentioning

confidence: 99%

First-spike latency information in single neurons increases when referenced to population onset

Chase

Young

2007

Proc. Natl. Acad. Sci. U.S.A.

168

147

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“…Higher up in the auditory system, Chase and Young (2005) studied the coding of multiple cues for space in cat inferior colliculus (IC). The question they addressed was that of segregation of processing pathways through the IC.…”

Section: Applications To the Auditory Systemmentioning

confidence: 99%

Information theory in auditory research

Nelken

Chechik

2007

Hearing Research

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Mutual information (MI) is in increasing use as a way of quantifying neural responses. However, it is still considered with some doubts by many researchers, because it is not always clear what MI really measures, and because MI is hard to calculate in practice. This paper aims to clarify these issues. First, it provides an interpretation of mutual information as variability decomposition, similar to standard variance decomposition routinely used in statistical evaluations of neural data, except that the measure of variability is entropy rather than variance. Second, it discusses those aspects of the MI that makes its calculation difficult. The goal of this paper is to clarify when and how information theory can be used informatively and reliably in auditory neuroscience.

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“…The central nucleus of the inferior colliculus (ICC) receives ascending input from nearly every major brainstem nucleus (Roth et al, 1978;Adams, 1979;Brunso-Bechtold et al, 1981;Oliver et al, 1997) and is one of the first sites of convergence for the three major sound-localization cues: interaural level differences (ILDs), interaural timing differences (ITDs), and monaural spectral cues (SNs for spectral notches). Previous work has shown that single ICC neurons display a range of sensitivity to localization cues, and most of the neural responses are modulated by more than one cue (Benevento and Coleman, 1970;Caird and Klinke, 1987;Delgutte et al, 1995Delgutte et al, , 1999Chase and Young, 2005). This work, however, has all been based on the assumption of a rate code.…”

Section: Introductionmentioning

confidence: 97%

“…The analysis allows the time resolution of the temporal representation to be determined, suggesting that a temporal decoder would have to be sensitive to spike-timing coincidences of ϳ12 ms to extract maximum information. Temporal coding increases the degrees of freedom of the spike code in such a way that multiple stimulus features can be independently represented, which is not possible with only a rate code (Chase and Young, 2005).…”

Section: Introductionmentioning

confidence: 99%

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

Chase¹,

Young²

2006

J. Neurosci.

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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. Spiketiming-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.

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Limited Segregation of Different Types of Sound Localization Information among Classes of Units in the Inferior Colliculus

Abstract: The auditory system uses three cues to decode sound location: interaural time differences (ITDs), interaural level differences (ILDs), and spectral notches (

Cited by 65 publications

References 61 publications

First-spike latency information in single neurons increases when referenced to population onset

First-spike latency information in single neurons increases when referenced to population onset

Information theory in auditory research

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

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