Research Article: Multiplicative Auditory Spatial Receptive Fields Created by a Hierarchy of Population Codes

Date Published: November 24, 2009

Publisher: Public Library of Science

Author(s): Brian J. Fischer, Charles H. Anderson, José Luis Peña, Benedikt Grothe. http://doi.org/10.1371/journal.pone.0008015

Abstract: A multiplicative combination of tuning to interaural time difference (ITD) and interaural level difference (ILD) contributes to the generation of spatially selective auditory neurons in the owl’s midbrain. Previous analyses of multiplicative responses in the owl have not taken into consideration the frequency-dependence of ITD and ILD cues that occur under natural listening conditions. Here, we present a model for the responses of ITD- and ILD-sensitive neurons in the barn owl’s inferior colliculus which satisfies constraints raised by experimental data on frequency convergence, multiplicative interaction of ITD and ILD, and response properties of afferent neurons. We propose that multiplication between ITD- and ILD-dependent signals occurs only within frequency channels and that frequency integration occurs using a linear-threshold mechanism. The model reproduces the experimentally observed nonlinear responses to ITD and ILD in the inferior colliculus, with greater accuracy than previous models. We show that linear-threshold frequency integration allows the system to represent multiple sound sources with natural sound localization cues, whereas multiplicative frequency integration does not. Nonlinear responses in the owl’s inferior colliculus can thus be generated using a combination of cellular and network mechanisms, showing that multiple elements of previous theories can be combined in a single system.

Partial Text: The barn owl is able to pinpoint sound sources with great accuracy after hearing only a short burst of sound [1]. This orienting response is mediated by spatially-selective auditory neurons in the midbrain [2], [3]. Spatial selectivity arises in these auditory neurons as a result of computations performed on the auditory input signals (for review see, [4], [5]). Multiplication is believed to be an essential computation in the generation of spatially selective auditory neurons in the owl’s midbrain [6], [7].

We present a model for the emergence of auditory spatial tuning in ITD- and ILD-sensitive neurons of the barn owl’s ICx (Figure 2). ITD- and ILD-dependent cues are extracted from auditory input signals at an array of frequencies using cross-correlation and level-subtraction, respectively. The ITD- and ILD-dependent cues form the input to a network of spiking neurons that model two regions of the inferior colliculus where ITD- and ILD-sensitive neurons are found, ICx and its afferent neurons in ICcl. We assume that the nonlinear spiking responses to ITD and ILD found in ICcl [7] are produced by a nonlinear-additive mechanism [43], [44]. That is, we assume that in ICcl, ITD- and ILD-dependent cues within frequency channels are combined additively in the membrane potential and are transformed to a nonlinear spiking response by the spiking input-output function. The subthreshold responses of ICx neurons can then be described as a sum across frequency of products of ITD- and ILD-dependent functions. The network model describes how a linear combination of the responses of populations of ICcl neurons can compute the products of ITD- and ILD-dependent functions, and thereby produces the experimentally observed responses to ITD and ILD in ICx.

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http://doi.org/10.1371/journal.pone.0008015

 

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