Brain bases for navigating acoustic features

Abstract

Whether physical navigation shares neural substrates with mental travel in other behaviourally relevant domains is debated. With respect to sound, pure-tone working memory in humans elicits hippocampal as well as auditory cortical and inferior frontal activity, and rodent work suggests that hippocampal cells that usually track an animal's physical location can also map to tone frequency when task-relevant. We generated a sound dimension based on the density of random-frequency tones in a stack, resulting in a percept ranging from low- ("beepy") to high-density ("noisy"). We established that unlike tone frequency, which listeners automatically associate with vertical position, this density dimension elicited no consistent spatial mapping. During functional magnetic resonance imaging, human participants held in mind the density of a series of tone stacks and, after a short maintenance period, adjusted further stacks to match the target ("navigation"). Density of the currently heard sound was represented most strongly in bilateral non-primary auditory cortex, specifically bilateral planum polare, while density of the maintained target was represented in right anterior hippocampus and left inferior temporal gyrus. Encoding and maintenance activity in bilateral hippocampus, inferior frontal gyrus, planum polare and posterior cingulate was positively associated with subsequent navigation success. Bilateral inferior frontal gyrus and hippocampus were among regions with elevated activity during adjustment, compared to a parity-judgment condition with closely matched acoustics and motor demands. Bilateral orbitofrontal cortex was more active when navigation was toward a target density than when participants adjusted density in a control condition with no particular target. We find that self-initiated travel along a non-spatial auditory dimension engages a brain system overlapping with that supporting physical navigation.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

* Replaced all within-participant multivariate analyses with across-participant multivariate analyses. Main results results were unchanged, but a representation of the target density was also found in right anterior hippocampus and left inferior temporal gyrus. Other minor changes to figures and discussion.

* https://openneuro.org/datasets/ds006211

Funder Information Declared

Wellcome Trust, https://ror.org/029chgv08, WT106964MA, 203147/Z/16/Z

Medical Research Council, MR/T032553/1