Neural Correlates of the Precedence Effect in the Inferior Colliculus: Effect of Localization Cues

Abstract

Litovsky, R. Y. and B. Delgutte. Neural correlates of the precedence effect in the inferior colliculus: effect of localization cues. J Neurophysiol 87: 976 -994, 2002; 10.1152/jn.00568.2001. The precedence effect (PE) is an auditory phenomenon involved in suppressing the perception of echoes in reverberant environments, and is thought to facilitate accurate localization of sound sources. We investigated physiological correlates of the PE in the inferior colliculus (IC) of anesthetized cats, with a focus on directional mechanisms for this phenomenon. We used a virtual space (VS) technique, where two clicks (a "lead" and a "lag") separated by a brief time delay were each filtered through head-related transfer functions (HRTFs). For nearly all neurons, the response to the lag was suppressed for short delays and recovered at long delays. In general, both the time course and the directional patterns of suppression resembled those reported in freefield studies in many respects, suggesting that our VS simulation contained the essential cues for studying PE phenomena. The relationship between the directionality of the response to the lead and that of its suppressive effect on the lag varied a great deal among IC neurons. For a majority of units, both excitation produced by the lead and suppression of the lag response were highly directional, and the two were similar to one another. For these neurons, the long-lasting inhibitory inputs thought to be responsible for suppression seem to have similar spatial tuning as the inputs that determine the excitatory response to the lead. Further, the behavior of these neurons is consistent with psychophysical observations that the PE is strongest when the lead and the lag originate from neighboring spatial locations. For other neurons, either there was no obvious relationship between the directionality of the excitatory lead response and the directionality of suppression, or the suppression was highly directional whereas the excitation was not, or vice versa. For these neurons, the excitation and the suppression produced by the lead seem to depend on different mechanisms. Manipulation of the directional cues (such as interaural time and level differences) contained in the lead revealed further dissociations between excitation and suppression. Specifically, for about one-third of the neurons, suppression depended on different directional cues than did the response to the lead, even though the directionality of suppression was similar to that of the lead response when all cues were present. This finding suggests that the inhibitory inputs causing suppression may originate in part from subcollicular auditory nuclei processing different directional cues than the inputs that determine the excitatory response to the lead. Neurons showing such dissociations may play an important role in the PE when the lead and the lag originate from very different directions.

Neural correlates of the precedence effect in auditory evoked potentials

“…For single neurons of the IC in the cat, Yin (1994) found a median lead-lag delay of 20 ms for a 50% recovery. Similar results were obtained by Litovsky et al (2001) and Litovsky and Delgutte (2002) (lead-lag delay 32 ms). Fitzpatrick et al (1999) found increasing lead-lag delays for a 50% recovery in structures of the ascending auditory pathway (from the auditory nerve up to the cortex) in cats and rabbits.…”

“…Single cell studies were made in different species, e.g., in the external colliculus of the inferior colliculus of the barn owl (Keller and Takahashi, 1996), the inferior colliculus (IC) of the rabbit (Fitzpatrick et al, 1995) and the IC of the cat (Litovsky, 1998;Litovsky and Yin, 1998;Litovsky and Delgutte, 2002;Yin, 1994) and revealed that correlates of the precedence effect already exist on the level of the IC. Response rates of single neurons depend similarly on the direction of lead and lag sources and the lead-lag delay as the perceived location of the compound stimulus (lead and lag) in corresponding behavioral tasks performed by humans or cats (see, e.g., Tollin and Yin, 2003).…”

“…However, a more recent study (Litovsky and Delgutte, 2002) revealed that neural correlates of the precedence effect are highly related to localization cues. Applying a virtual space technique, they found that, for a majority of IC neurons, the excitation produced by the lead as well as the suppression of the lag response strongly depended on directional cues.…”

Physiological and Psychophysical Modeling of the Precedence Effect

“…The parameters for the ipsilateral and contralateral excitatory synaptic conductances, including the number of input neurons, the maximum value and the time constant of the synaptic conductance, and the delay of the input arrival, are identical to those used in Brughera et al (1996) (Kuwada and Yin 1983;Carney and Yin 1989;Loftus et al 2004). Delayed inhibitory inputs to the IC from DNLL are thought to contribute to the neural correlates of the PE (Carney and Yin 1989;Yin 1994;Fitzpatrick et al 1995;Litovsky and Yin 1998a, b;Litovsky and Delgutte 2002).…”

“…The population consisted only of SMAX units because SMAX units are thought to be more prevalent in the auditory pathway (Litovsky and Yin 1998b;Litovsky and Delgutte 2002). We used this population to simulate the results of behavioral experiments in which subjects were asked to indicate the perceived location(s) of the lead/lag target by adjusting the ITD of a pointer stimulus (Litovsky and Shinn-Cunningham 2001).…”