Is Human Auditory Cortex Organization Compatible With the Monkey Model? Contrary Evidence From Ultra-High-Field Functional and Structural MRI

Abstract

It is commonly assumed that the human auditory cortex is organized similarly to that of macaque monkeys, where the primary region, or “core,” is elongated parallel to the tonotopic axis (main direction of tonotopic gradients), and subdivided across this axis into up to 3 distinct areas (A1, R, and RT), with separate, mirror-symmetric tonotopic gradients. This assumption, however, has not been tested until now. Here, we used high-resolution ultra-high-field (7 T) magnetic resonance imaging (MRI) to delineate the human core and map tonotopy in 24 individual hemispheres. In each hemisphere, we assessed tonotopic gradients using principled, quantitative analysis methods, and delineated the core using 2 independent (functional and structural) MRI criteria. Our results indicate that, contrary to macaques, the human core is elongated perpendicular rather than parallel to the main tonotopic axis, and that this axis contains no more than 2 mirror-reversed gradients within the core region. Previously suggested homologies between these gradients and areas A1 and R in macaques were not supported. Our findings suggest fundamental differences in auditory cortex organization between humans and macaques.

Improving a probabilistic cytoarchitectonic atlas of auditory cortex using a novel method for inter-individual alignment

“…Te1.0) could be leveraged by considering single subjects in the future ( Moerel et al, 2014 ). Te2.2 captured the most posterior portion of the larger tonotopic gradient that, consistently with previous reports, we identify as running in a direction orthogonal to Heschl’s Gyrus ( Moerel et al, 2014; Besle et al, 2018 ). The other cyto-architectonic regions that overlapped with our functional acquisition field of view (Te2.1 and Te3) covered low frequency preferring regions of the tonotopic map in the lateral portion of the Heschl’s sulcus and the superior temporal gyrus.…”

“…These results argue for the necessity of interpreting large scale tonotopic maps which alone do not allow defining the borders between cortical areas ( Moerel et al, 2014 ). A large tonotopic gradient unarguably runs in a posterior to anterior direction Da Costa et al (2011 ); Besle et al (2018 ). Equating this gradient with the gradient that identifies the primary auditory cortex results in a view in which the core lies orthogonal to Heschl’s Gyrus ( Da Costa et al, 2011; Saenz and Langers, 2014; Besle et al, 2018 ).…”

“…A large tonotopic gradient unarguably runs in a posterior to anterior direction Da Costa et al (2011 ); Besle et al (2018 ). Equating this gradient with the gradient that identifies the primary auditory cortex results in a view in which the core lies orthogonal to Heschl’s Gyrus ( Da Costa et al, 2011; Saenz and Langers, 2014; Besle et al, 2018 ). On the other hand, the cyto-architectonic areas-now restricted in size by better aligning macro-anatomy-suggest that the auditory core (Te1) runs along Heschl’s Gyrus (i.e.…”

“…We showcase this approach by applying CBA+ to an in vivo dataset collected at 7 Tesla and projecting the improved cyto-architectonic atlas onto functional and anatomical group maps. In addition, in order to contribute to the ongoing debate on the in vivo localization of auditory cortical areas ( Moerel et al, 2014; Besle et al, 2018 ), we align the cyto-architectonic atlas (and in vivo data) to a recent temporal lobe parcellation based on in vivo measurements ( Glasser et al, 2016 ).…”

Imaging the human auditory system at ultrahigh magnetic fields

“…Following the invention of fMRI, Binder et al (1994) first conducted an auditory study focused only on the cortex. It took a few years until Guimaraes et al (1998) to investigate the subcortical auditory system.…”