Frequency representation within the human brain: stability versus plasticity

Abstract

A topographical representation for frequency has been identified throughout the auditory brain in animals but with limited evidence in humans. Using a midbrain implant, we identified an ordering of pitch percepts for electrical stimulation of sites across the human inferior colliculus (IC) that was consistent with the IC tonotopy shown in animals. Low pitches were perceived by the subject for stimulation of superficial IC sites while higher pitches were perceived for stimulation of deeper sites. Interestingly, this pitch ordering was not initially observed for stimulation across the IC, possibly due to central changes caused by prior hearing loss. Daily implant stimulation for about 4 months altered the pitch percepts from being predominantly low to exhibiting the expected ordering across the stimulated IC. A presumably normal tonotopic representation may have been maintained within the IC or accessible through IC stimulation that helped form this pitch ordering perceived in higher centers.

Figure 1. Electrode array implantation across the right ICC.

(a) The array consists of 20 platinum ring electrodes linearly spaced at 200 μm along a silicone carrier. Each site has a thickness of 100 μm and an area of 0.126 mm². A stainless steel stylet through the center of the silicone array enables insertion into the brain and is removed after proper array placement. (b) Parasagittal (middle) and axial (right) sections show the location of the array (black line). An arrow in the parasagittal section points to the caudal-rostral location of the array and also corresponds to the location of the axial section shown to the right derived from CT and MRI images superimposed onto fixed human midbrain slices. The array spans the expected low to high frequency gradient from the superficial to deeper layers of the ICC (dorsal-caudal portion) based on animal studies. Right ICC stimulation elicited sounds perceived as coming from the left ear. The tip sites 12 to 20 were located in deeper non-auditory regions (e.g., periaqueductal gray, PAG) and were inactivated. Images in this figure were taken from previous publications and reprinted with permission from Society for Neuroscience and Wolters Kluwer Health. ICD: dorsal cortex of inferior colliculus, C: caudal, D: dorsal, R: rostral, V: ventral.

Figure 2. Pitch ordering over time for three different tests.

(a) Subject indicated a value from 0 to 5 for each stimulated site based on a pitch scale of familiar objects (0: bass or boat horn, 2: man's voice, 3.5: woman's voice, 5: bird chirping). Average and standard deviation across n trials are plotted for each site (1.5 mo: n = 5, 10 mo: n = 10, 21 mo: n = 5). Asterisks denote significantly higher 10- and 21-month values than 1.5-month values (p < 0.006, two-tailed ranked unequal variance t-test). (b) Two-alternative forced choice (2-AFC) ranking method required the subject to indicate which site out of two sequentially stimulated sites had a higher pitch. All sites were then rank ordered based on how often each site had a higher pitch over all other sites (in percentage). Each site pair was compared n times (1 wk: n = 12, 4 mo: n = 4, 10 mo: n = 20, 13 mo: n = 10, 35 mo: n = 4). (c) Subject indicated a number from 0 to 50 (low to high pitch) for each site. Average and standard deviation across n trials is plotted for each site (two sessions for 1 wk: n = 10 each, 1.5 mo: n = 5). For each test, all sites were stimulated in a random sequence and at a similar loudness level. Site 7 was shorted to a non-auditory site and was excluded.

Figure 3. Activation levels over time.

Threshold and upper comfortable levels were measured in terms of total charge per phase of the biphasic pulses presented on each site and plotted as a vertical line with a symbol at the midpoint. Site 7 was electrically shorted to a distant non-auditory site and required higher activation levels. Levels generally increased over time, but there were no systematic differences in the values or change in values for the deeper sites compared to the shallower sites. It would be expected that if there was greater damage and/or recovery of neurons surrounding the deeper sites (i.e., sites 8 – 11), then activation levels should have been higher and/or levels should have changed differently over time compared to the shallower sites.

Figure 4. The expected pitch ordering produced by non-tonotopic activation of the right ICC.

(a) Hearing thresholds for the left ear before deafness onset caused by acoustic neuroma removal surgery. Sounds entering the left ear project predominantly to the right ICC. (b) Different frequency components (between LowF to HighF in Hz) of incoming sound are electrically presented on each site for daily implant use. Non-tonotopic activation across the right ICC (i.e., without a systematic ordering of sites that matches the tonotopy of the ICC shown in animal studies) during the first 10 months of stimulation produced the expected pitch ordering shown in Fig. 2 that was supposedly altered by the high frequency hearing loss shown in (a).