The organization of frequency and binaural cues in the gerbil inferior colliculus

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The central nucleus of the inferior colliculus (IC) is the common target of separate ascending pathways that convey discrete types of auditory information (for reviews, see Hutson, 1997; Winer & Schreiner, 2005; for more recent studies, see Malmierca, Saint Marie, Merchan, & Oliver, 2005; Cant & Benson, 2006; Loftus, Bishop, & Oliver, 2010; Cant, 2013; Felix, Magnusson, & Berrebi, 2015). From there, the information is relayed to the ventral division of the medial geniculate body (MGv) of the thalamus, which in turn projects to multiple core regions of the auditory cortex, including the primary auditory cortex (AI). A transformation from an organization based on frequency to one according to function occurs between the level of the IC and the auditory cortex. This transformation is best shown in the mustached bat, where neurons with different physiological properties and functional roles, such as sensitivity to target range or relative velocity, are arrayed according to their position in the tonotopic map of the IC central nucleus (Wenstrup, Mittmann, & Grose, 1999; Portfors & Wenstrup, 2001). However, at the level of the cortex, neurons are clustered into functional areas characterized by a common response type (O'Neill & Suga, 1979; Suga, O'Neill, Kujirai, & Manabe, 1983; Fitzpatrick, Suga, & Olsen, 1998). In other mammals, the isofrequency laminae in the IC become multiple tonotopic regions in the cortex. Functional parcellation of the cortical areas is likely, such as into “place” and “pattern” pathways (Malhotra, Hall, & Lomber, 2004; Lomber & Malhotra, 2008; Recanzone & Cohen, 2010; Rauschecker, 2015), but the details of these functional areas are less clear than in the mustached bat. In addition, in the mustached bat the change from an organization according to frequency to one according to function occurs in the output pathways of the IC, so that the thalamic organization resembles that seen in the cortex (Olsen & Suga, 1991a, 1991b; Wenstrup, Larue, & Winer, 1994; Wenstrup & Grose, 1995; Wenstrup, 1999; Pearson, Crocker, & Fitzpatrick, 2007). In other species, the connection from the IC to the thalamus is typically presented as a single pathway, and the output from the thalamus as branching to innervate separate cortical areas (Kaas & Hackett, 2000; Winer & Schreiner, 2005). These relationships are schematized in Figure 1. Other than in the mustached bat, pathways from the IC to the thalamus are not typically described in terms of both physiological and functional roles—in part due to the lack of identified “information‐bearing parameters” that relate specific responses and neuronal location to a functional role. An exception is sensitivity to interaural time difference (ITD), which is an information‐bearing parameter for sound location as well as for improving signal detection in noise.
Processing of ITDs in terms of neurophysiology and behavior is among the most studied properties of the auditory system (Bernstein, 2001; Konishi, 2003; Palmer & Kuwada, 2005; Vonderschen & Wagner, 2014). Most of the physiological focus has been on identifying the specializations used in pathways from the auditory nerve to the superior olivary complex (SOC) to encode and extract the ITD information with microsecond resolution. Less attention has been paid to localization of ITD‐sensitive neurons within the pathways from the IC to the cortex than to the physiological properties of the neurons. Here, we used gerbils to study the localization of ITD sensitivity within the IC. Previous studies on gerbil ITD sensitivity have described the pathways to the IC from the main nuclei of the SOC that convey ITD information (Cant & Benson, 2006; Cant, 2013).
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