Orthogonal acoustic dimensions define auditory field maps in human cortex

Abstract

The functional organization of human auditory cortex has not yet been characterized beyond a rudimentary level of detail. Here, we use functional MRI to measure the microstructure of orthogonal tonotopic and periodotopic gradients forming complete auditory field maps (AFMs) in human core and belt auditory cortex. These AFMs show clear homologies to subfields of auditory cortex identified in nonhuman primates and in human cytoarchitectural studies. In addition, we present measurements of the macrostructural organization of these AFMs into "clover leaf" clusters, consistent with the macrostructural organization seen across human visual cortex. As auditory cortex is at the interface between peripheral hearing and central processes, improved understanding of the organization of this system could open the door to a better understanding of the transformation from auditory spectrotemporal signals to higher-order information such as speech categories.tonotopy | periodotopy | cochleotopy | temporal receptive field | traveling wave H umans have evolved a highly sophisticated auditory system for the transduction and analysis of acoustic information, such as the spectral content of sounds and the temporal modulation of sound energy. The basilar membrane of the cochlea is organized tonotopically to represent the spectral content of sounds from high to low frequencies. This tonotopic (or cochleotopic) organization is preserved as auditory information is processed and passed on from the cochlea to the superior olive, the inferior colliculus, the medial geniculate nucleus, and into primary auditory cortex. Such cortical preservation of the peripheral sensory topography creates a common topographic sensory matrix in hierarchically organized sensory systems, important for consistent sensory computations. The current state of knowledge of the functional organization of human auditory cortex indicates the existence of multiple cortical subfields organized tonotopically. However, the number of these human cortical subfields, their boundaries, and their orientations relative to anatomical landmarks remain equivocal, due in part to an inability to measure cortical representations of a second acoustic dimension orthogonal to tonotopy to accurately delineate them.This ambiguity of human auditory subfield definitions contrasts dramatically with the current understanding of the functional organization of human visual cortex, in which detailed maps of the organization of the retina, called visual field maps (VFMs), have been well characterized (1-9). In vision, there are two orthogonal dimensions of visual space, eccentricity and polar angle, which together allow for the mapping of cortical representations to unique locations in visual space and the complete delineation of the boundaries of individual visual field maps. In audition, there has been only one dimension of sensory topography clearly mapped in cortex, which makes it impossible to use sensory topography to accurately differentiate specific human cortical auditory field maps (AFM...

Reconstructing the spectrotemporal modulations of real-life sounds from fMRI response patterns

“…Our current findings indicate that spectrotemporal sound modulations also map into distinct and reproducible spatial fMRI response patterns. This result is consistent with the hypothesis of a spatial representation of acoustic features besides frequency in primate (31) and human (14,15,32) auditory cortex.…”

BOLD fMRI study of ultrahigh frequency encoding in the inferior colliculus

“…Recent development in BOLD fMRI has been demonstrated for studying the rodent auditory system (Cheung et al, 2012a(Cheung et al, , 2012bGao et al, 2014;Lau et al, 2013Lau et al, , 2015Yu et al, 2009;Zhang et al, 2013), along with previous auditory fMRI studies conducted on humans (Barton et al, 2012;De Martino et al, 2013;Sigalovsky and Melcher, 2006), primates (Baumann et al, 2011;Kayser et al, 2007;Tanji et al, 2010) and songbirds (Boumans et al, 2007;Van Meir et al, 2005;Voss et al, 2007).…”

Visual Objects in the Auditory System in Sensory Substitution: How Much Information Do We Need?

“…If auditory object recognition is a limiting factor, then information process ing in primary auditory cortex is crucial; phase locking in auditory cortex is limited to around 30 Hz, thus we would expect a ceiling effect at the 16 x 16 image resolution (Barton et al, 2012). However, the ceiling effect at 8 x 8 pixels suggests that object recognition is instead processed further up the auditory pathway, such as in the superior temporal gyms (STG) where phase locking is reduced to <16 Hz.…”

“…Phase-locking on the auditory nerve is limited to around 4000 Hz (Joris et al, 2004). By midbrain (inferior colliculus) this limit is reduced to around 300 Hz (Baumann et al, 2011;Joris et a l, 2004) and by primary auditory cortex it is further reduced to around 30 Hz (Barton et al, 2012). In superior temporal gyrus (part of Wernicke's speech area), this limit is further reduced to < 16 Hz in the object-based rep resentation of speech (Pasley et al, 2012), which limits coincide with those established in human psychoacoustic studies Simp son et al, 2013).…”

“…Such acoustic features are encoded inde pendently in the peripheral auditory system and object-based representations emerge in primary auditory cortex (Ding and Simon, 2012;Mesgarani and Chang, 2012;Shamma et al, 2011;Teki et al, 2013). Auditory cortex main tains a two-dimensional topographic map of frequency (Humphries et al, 2010) and modulation-rate (Barton etal., 2012) that are the so-called tonotopic and periodotopic axes, where individual regions on the map independently represent sound features occurring at a specific frequency and modulation rate (Barton et al, 2012;Simon and Ding, 2010;Xiang et al, 2013). It is thought that auditory objects are formed, in cortex, according to temporal coherence between these independently-coded acoustic features (Shamma et al, 2011;Teki et al, 2013).…”