Navigating the auditory scene: an expert role for the hippocampus

Abstract

Over a typical career piano tuners spend tens of thousands of hours exploring a specialized acoustic environment. Tuning requires accurate perception and adjustment of beats in two-note chords that serve as a navigational device to move between points in previously learned acoustic scenes. It is a two-stage process that depends on the following: first, selective listening to beats within frequency windows, and, second, the subsequent use of those beats to navigate through a complex soundscape. The neuroanatomical substrates underlying brain specialization for such fundamental organization of sound scenes are unknown. Here, we demonstrate that professional piano tuners are significantly better than controls matched for age and musical ability on a psychophysical task simulating active listening to beats within frequency windows that is based on amplitude modulation rate discrimination. Tuners show a categorical increase in gray matter volume in the right frontal operculum and right superior temporal lobe. Tuners also show a striking enhancement of gray matter volume in the anterior hippocampus, parahippocampal gyrus, and superior temporal gyrus, and an increase in white matter volume in the posterior hippocampus as a function of years of tuning experience. The relationship with gray matter volume is sensitive to years of tuning experience and starting age but not actual age or level of musicality. Our findings support a role for a core set of regions in the hippocampus and superior temporal cortex in skilled exploration of complex sound scenes in which precise sound "templates" are encoded and consolidated into memory over time in an experience-dependent manner.

Figure 1.

Active listening to beats within particular spectral windows. A, Detection of beats in a spectral window for a two-note piano chord. A perfect fifth is shown between the notes C (red) and G (blue). This interval is so called because it spans five positions on the musical staff and corresponds to a seven-semitone pitch difference. When the popular equal-temperament tuning is used, in which the octave is divided into 12 exactly equal intervals, this corresponds to a pitch ratio of 2^7/12 that is approximately, but not exactly, equal to 1.5. This means that there is near coincidence of the third (and sixth) harmonic of C and the second (and fourth) harmonic of G. Because the harmonics do not coincide exactly beating occurs between them. For clarity, the beat amplitudes are shown as having the same intensity: the actual spectrum of piano notes shows increasing attenuation of the higher harmonics. The time waveform of the third harmonic of C (red) and second harmonic of G (blue) are shown below where they interact to demonstrate beat production as indicated by the amplitude modulated black waveform (envelope shown in green). Piano tuners are therefore required to listen selectively to beat rates that only occur in particular spectral windows and to adjust the beat rates to prescribed values (typically <20 Hz: Table 1) that specify the intervals. In this experiment, we tested a generic basis for this skill by requiring subjects to detect changing amplitude modulation of the third harmonic of a five-harmonic complex using beat rates within the range used by tuners (AM rate discrimination task). B, Mean thresholds for 19 piano tuners (depicted in blue) and 19 controls (depicted in green) are shown for the AM rate discrimination task at 2 Hz (3.26 ± 0.32% vs 4.17 ± 0.32%), 16 Hz (3.88 ± 0.57% vs 6.93 ± 0.60%), and a control task based on pure tone frequency discrimination (0.44 ± 0.10% vs 1.02 ± 0.33%). Mean thresholds for the 2 Hz and 16 Hz AM tasks were significantly different between the two groups while there was no significant difference between groups on the frequency discrimination task (see Results). Error bars indicate ±1 SE. C, Enhanced GM volume in piano tuners was found in the right planum polare and frontal operculum as shown in the sagittal section at x = 42. Greater GM volume in the frontal operculum is shown in the coronal section at y = 20. The strength of changes in GM volume (t value) is graded according to the color scheme on the right and shown at p < 0.001 (uncorrected).

Figure 2.

Navigation through a remembered piano soundscape. A, One algorithm for navigating the piano soundscape using successive two-note chords—a tuning sequence of rising perfect fifths and falling perfect fourths starting on C and ending on B# immediately above the starting C. Different piano tuners use different schemes. B, Significantly greater GM volume as a function of years of piano tuning experience was found in the right anterior hippocampus as shown on a coronal section at y = −17. The significance of this change in GM volume (t value) is graded according to the color scheme next to the figure and shown at p < 0.001 (uncorrected). C, Significantly greater WM volume as a function of years of piano tuning experience was found in the posterior hippocampus bilaterally as shown on a coronal section at y = −24. The significance of this change in WM volume (t value) is graded according to the color scheme next to the figure and shown at p < 0.001 (uncorrected). D, A significant positive correlation was found between the GM volume changes in the right anterior hippocampus and years of piano tuning (r = 0.43; p < 0.05).