Reconsidering Tonotopic Maps in the Auditory Cortex and Lemniscal Auditory Thalamus in Mice

Abstract

The auditory thalamus and auditory cortex (AC) are pivotal structures in the central auditory system. However, the thalamocortical mechanisms of processing sounds are largely unknown. Investigation of this process benefits greatly from the use of mice because the mouse is a powerful animal model in which various experimental techniques, especially genetic tools, can be applied. However, the use of mice has been limited in auditory research, and thus even basic anatomical knowledge of the mouse central auditory system has not been sufficiently collected. Recently, optical imaging combined with morphological analyses has enabled the elucidation of detailed anatomical properties of the mouse auditory system. These techniques have uncovered fine AC maps with multiple frequency-organized regions, each of which receives point-to-point thalamocortical projections from different origins inside the lemniscal auditory thalamus, the ventral division of the medial geniculate body (MGv). This precise anatomy now provides a platform for physiological research. In this mini review article, we summarize these recent achievements that will facilitate physiological investigations in the mouse auditory system.

Keywords: auditory cortex; brain map; medial geniculate body; mice; multiple compartments; thalamocortical pathway; tonotopy; topology.

Figure 1

A new map of the mouse auditory cortex visualized using flavoprotein fluorescence imaging (FFI). (A) A quantitative surface map of the six subregions of the mouse AC revealed using FFI. These panels were modified from Tsukano et al. (2016). AC, auditory cortex; Cb, cerebellum; MCA, medial cerebral artery; OB, olfactory bulb; RF, rhinal fissure; SC, somatosensory cortex; VC, visual cortex. (B) Illustration of the original map (Stiebler et al., 1997) and a map based on the results of recent optical imaging studies (Sawatari et al., ; Tsukano et al., 2015). These AC maps are considered to reflect a map lying in layers 2/3. (C) Delineation of the six auditory subregions in the coronal view. Bar, 1 mm. These panels were modified from Tsukano et al. (2016).

Figure 2

The remodeled thalamocortical auditory pathway in mice. (A) Schematic drawing of the thalamocortical auditory pathway. The AC receives thalamic inputs from the ventral division of the medial geniculate body (MGv). (B) Multiple compartments revealed inside of the MGv. Neurons projecting to the dorsomedial field (DM) are localized in the rostral compartment (red; Tsukano et al., 2015). Neurons projecting to the primary auditory cortex (A1) are localized in the lateral compartment of the middle MGv (green; Horie et al., ; Takemoto et al., 2014). Neurons projecting to the anterior auditory field (AAF) are localized in the medial compartment of the middle MGv (blue; Horie et al., ; Takemoto et al., 2014). Neurons projecting to the insular auditory field (IAF) are localized in the inferomedial compartment in the middle MGv (yellow; Takemoto et al., 2014). Each compartment gives rise to topological projections to its cortical target. In addition, the caudal half of the mouse MGv is now uncharacterized (Tsukano et al., 2015); therefore, it is highly possible that neurons projecting to the secondary auditory field (A2), a remaining tonotopic region in the AC, are localized in the caudal MGv compartment as suggested in Ohga et al. (2015). (C) A new model of the thalamocortical auditory pathway, which is composed of several parallel streams. Future studies are necessary to determine whether the central nucleus of the inferior colliculus (ICc) is also composed of multiple compartments with a distinct frequency organization, or whether divergence of tonotopy from the ICc to the MGv occurs. Moreover, whether that the caudal compartment in the MGv is arranged topographically is not clear. Comp, compartment.