A Missing Connection: A Review of the Macrostructural Anatomy and Tractography of the Acoustic Radiation

Abstract

The auditory system of mammals is dedicated to encoding, elaborating and transporting acoustic information from the auditory nerve to the auditory cortex. The acoustic radiation (AR) constitutes the thalamo-cortical projection of this system, conveying the auditory signals from the medial geniculate nucleus (MGN) of the thalamus to the transverse temporal gyrus on the superior temporal lobe. While representing one of the major sensory pathways of the primate brain, the currently available anatomical information of this white matter bundle is quite limited in humans, thus constituting a notable omission in clinical and general studies on auditory processing and language perception. Tracing procedures in humans have restricted applications, and the in vivo reconstruction of this bundle using diffusion tractography techniques remains challenging. Hence, a more accurate and reliable reconstruction of the AR is necessary for understanding the neurobiological substrates supporting audition and language processing mechanisms in both health and disease. This review aims to unite available information on the macroscopic anatomy and topography of the AR in humans and non-human primates. Particular attention is brought to the anatomical characteristics that make this bundle difficult to reconstruct using non-invasive techniques, such as diffusion-based tractography. Open questions in the field and possible future research directions are discussed.

Keywords: acoustic radiation; auditory pathways; auditory system; auditory tract; diffusion-based tractography; sensory pathways.

FIGURE 1

A schematic representation of the ascending human auditory system. The auditory information enters through the auditory nerve and reaches the cochlear nucleus. From here, various projections transmit the information to different brainstem relays of both hemispheres and then to the auditory cortex. The lemniscal pathway is represented by solid lines; the extra-lemniscal pathway by dashed lines. CN, cochlear nucleus; SOC, superior olivary complex; LL, lateral lemniscus; Ic, inferior culliculus; MGN, medial geniculate nucleus; AR, acoustic radiation.

FIGURE 2

The image shows the acoustic radiation fibers in the rhesus monkey. The lesion (L) was located in the posterior thalamus. From here we can see numerous thalamocortical (or somato sensory) (sr) and auditory (ar) fibers emerging. The sr and the ar fibers form a system of which the ar occupies the most ventral position. The acoustic radiation occupies the upper half of the white matter of the superior temporal convolution (T1) and enters the cortex of the lower wall of the Sylvian fissure (FS). The level of this figure is immediately behind the posterior extremity of the lentiform nucleus; the entire length of the acoustic radiation is visible here. Cgm, medial geniculate nucleus; Cgl, lateral geniculate nucleus (adapted from Polyak, 1932; https://archive.org, public domain).

FIGURE 3

(A) Schematic representation of the projection fibers of the human brain (coronal view). (B) Coronal cut through the middle section of the thalamus. (C) Axial section of the brain; cut through the inferior thalamus. In the three panels, fibers belonging to the acoustic radiation have been highlighted in green and fibers of the internal capsule in pink. The acoustic radiation projects from the thalamus (TH) to the first temporal circonvolution (T1) and passes through the sub-lenticular and posterior segment of the internal capsule. This map clearly highlights the crossing between these two fiber systems. CC, Corpus callosum; EC, external capsule; ICPL, Posterior limb of the internal capsule; ICSL, sub-lenticular part of the internal capsule; CR, corona radiata; LGN, lateral geniculate nucleus; MGN, medial geniculate nucleus; T1, first temporal circonvolution; TH, thalamus (adapted from Dejerine and Dejerine-Klumpke, 1895; https://archive.org, public domain).

FIGURE 4

The tractography reconstruction of the acoustic radiation (AR) in three different studies. (A) 3D volumetric reconstruction of the right AR in one subject using a multi-tensor model and probabilistic tractography. Voxels are color-coded from 10 (red) to 50 (yellow) samples passing through the voxel (adapted with permission from Behrens et al., 2007). (B) The panel shows the streamlines of the right AR in axial view, as reconstructed in one subject using q-ball imaging and probabilistic tractography. The location of the thalamus and auditory cortex (AC) are specified by the blue boxes. The figure also shows the orientation distribution functions (ODF) corresponding to the inferior longitudinal fasciculus (ILF), highlighted by the green arrow (adapted with permissions from Berman et al., 2013). (C) Left: 3D tractography reconstruction of the right AR in one subject using constrained spherical deconvolution models and probabilistic tractography. A 3D rendering of the thalamus is also shown in gray and the borders of HG in green. Right: Klinger’s post-mortem blunt dissection of the right AR (modified from Maffei et al., 2018). In all three panels the location of thalamus (blue arrow) and auditory cortex (white arrow) are highlighted.