Neural Correlates of the Precedence Effect in the Inferior Colliculus of Behaving Cats

Abstract

Tollin, Daniel J., Luis C. Populin, and Tom C. T. Yin. Neural correlates of the precedence effect in the inferior colliculus of behaving cats. J Neurophysiol 92: 3286 -3297, 2004; doi:10.1152/ jn.00606.2004. Several auditory spatial illusions, collectively called the precedence effect (PE), occur when transient sounds are presented from two different spatial locations but separated in time by an interstimulus delay (ISD). For ISDs in the range of localization dominance (Ͻ10 ms), a single fused sound is typically located near the leading source location only, as if the location of the lagging source were suppressed. For longer ISDs, both the leading and lagging sources can be heard and localized, and the shortest ISD where this occurs is called the echo threshold. Previous physiological studies of the extracellular responses of single neurons in the inferior colliculus (IC) of anesthetized cats and unanesthetized rabbits with sounds known to elicit the PE have shown correlates of these phenomena though there were differences in the physiologically measured echo thresholds. Here we recorded in the IC of awake, behaving cats using stimuli that we have shown to evoke behavioral responses that are consistent with the precedence effect. For small ISDs, responses to the lag were reduced or eliminated consistent with psychophysical data showing that sound localization is based on the leading source. At longer ISDs, the responses to the lagging source recovered at ISDs comparable to psychophysically measured echo thresholds. Thus it appears that anesthesia, and not species differences, accounts for the discrepancies in the earlier studies. I N T R O D U C T I O NWhen transient sounds are presented from two locations and separated by an interstimulus delay (ISD), several spatial perceptual phenomena, collectively called the precedence effect (PE) (Wallach et al. 1949), occur. We have shown that cats experience each of these phenomena (Populin and Yin 1998; Tollin and Yin 2003a,b), an example of which is shown in Fig. 1. In cats, summing localization occurs for ISDs between about Ϯ400 s, where a single fused "phantom" sound is located between the sources but biased toward the sound source that is leading in time, which, for brevity, we will refer to in this paper simply as the "lead." Localization dominance occurs for ISDs of ϳ400 s to 10 ms, where the paired sounds are localized near the lead with little effect of the sound source that is lagging in time, which we will call the "lag," on localization. Finally, for ISDs more than ϳ10 ms, the echo threshold is reached, the shortest ISD at which the two separate sound source locations are first perceived. The mechanisms that produce the PE illusion are thought to be responsible for the ability to localize sounds accurately in natural echoic environments.The PE has been studied physiologically at virtually all levels of the auditory system, including the auditory nerve (Parham et al. 1996), the cochlear nucleus (Fitzpatrick et al. 1995; Parham et al. 1998;Wickesberg 1996),...

Inhibiting the Inhibition: A Neuronal Network for Sound Localization in Reverberant Environments

“…This is significant because the circuits that create the binaural properties of EE cells are different from those that create EI cells. One recent study from behaving cats showed suppression of responses to trailing sounds in high-frequency IC cells (Tollin et al, 2004). However, these cells responded briskly to sounds presented from the ipsilateral and contralateral side and therefore were not EI and not processed by the IID circuitry.…”

“…Previous studies concerned with physiological mechanisms of the precedence effect have been mainly conducted in the IC of rabbits and cats (Yin, 1994;Fitzpatrick et al, 1995Fitzpatrick et al, , 1999Litovsky and Delgutte, 2002;Tollin et al, 2004). In those studies, the response to the lagging sound was suppressed by the leading sound, and the studies focused on the interstimulus delay at which the lag responses recovered.…”

“…The periods of suppression of responses to trailing sounds in some types of IC cells is one feature that contributes to precedence (Yin, 1994;Fitzpatrick et al, 1995Fitzpatrick et al, , 1999Litovsky and Delgutte, 2002;Tollin et al, 2004). However, such a mechanism alone cannot account for the fact that the precedence effect is facultative.…”

Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil

“…Because our analysis showed that the IC response profile decays further under anesthesia, some reduction in average firing rate relative to awake IC is expected; however, it is not significant at the population level. The anesthetic regimen used in our study may account for the relatively minor anesthetic effects on IC response properties compared with some previous studies Tollin et al, 2004).…”

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“…The unit responded to each 100 s click in a train with distinct bursts of action potentials, which were folded on the 5 Hz period of the click train for presentation and analysis (Fig. 9A); the method is described in the study by Tollin et al (2004). That is, each click within a train was considered a single trial.…”