In marmosets with unilateral cochlear implants, we are investigating the neural representations of stimulation signals in auditory cortex, the effectiveness of various stimulation strategies, as well as the nature of developmental and experience-dependent plasticity related to cochlear implant usage.

Representations of Time-Varying Cochlear Implant Stimulation in Auditory Cortex of Awake Marmosets

(Johnson et al., 2017) In modern cochlear implant (CI) processors, the temporal information in speech or environmental sounds is delivered through modulated electric pulse trains. How the auditory cortex represents temporally modulated CI stimulation across multiple time scales has remained largely unclear. In this study, we compared directly neuronal responses in primary auditory cortex (A1) to time-varying acoustic and CI signals in awake marmoset monkeys (Callithrix jacchus). We found that A1 neurons encode both modalities using similar coding schemes, but some important differences were identified. Our results provide insights into mechanisms underlying how the brain processes sounds via a CI device and suggest a candidate neural code underlying rate–pitch perception limitations often observed in CI users.

Figure 7. Distribution of response boundaries, CI and acoustic. a, Synchronization boundaries of synchronized populations (CI, left, red; acoustic, right, blue). There was no significant difference between the distributions of synchronization boundaries (p = 0.253, WRS test, median CI = 41.2 Hz, median acoustic = 28.6 Hz). b, Scatterplot of synchronization boundaries in units with synchronized CI and acoustic responses (n = 22, r = 0.369, p = 0.091, Pearson) c, Rate–response boundaries of nonsynchronized populations. There was no significant difference between the distributions of rate–response boundaries (p = 0.356, WRS test, median CI = 64.2 Hz, median acoustic = 64.0 Hz). d, Scatterplot of rate–response boundaries in units with nonsynchronized CI and acoustic responses (n = 50, r = 0.613, p = 2.2e-6, Pearson) e, Combination of temporal and rate representations of the range of tested repetition rates. Each curve is the cumulative sum of the histograms representing the synchronized and nonsynchronized populations in a, or c, respectively. Dashed lines show the percentage of units with synchronization boundaries greater than or equal to a given repetition rates. Solid line shows the percentage of units with rate–response boundaries less than or equal to a given repetition rate.

Selective Neuronal Activation by Cochlear Implant Stimulation in Auditory Cortex of Awake Primate

(Johnson et al., 2016) The cochlear implant (CI) is the most successful neural prosthetic device to date and has restored hearing in hundreds of thousands of deaf individuals worldwide. However, despite its huge successes, CI users still face many perceptual limitations, and the brain mechanisms involved in hearing through CI devices remain poorly understood. By directly comparing single-neuron responses to acoustic and CI stimulation in auditory cortex of awake marmoset monkeys, we discovered that neurons unresponsive to CI stimulation were sharply tuned to frequency and sound level. Our results point out a major deficit in central auditory processing of CI stimulation and provide important insights into mechanisms underlying the poor CI user performance in a wide range of perceptual tasks.

Figure 1. Topographic maps of auditory cortex responses to acoustic and CI stimulation. A, Acoustic BF maps of left and right auditory cortex (AC) of a marmoset implanted unilaterally in the right cochlea with a CI electrode array (inset plot). Dashed lines indicate approximate positions of the lateral sulcus. Each circle represents a single neuron recorded at that cortical surface location, color-coded by its BF. Black open circles represent neurons nonresponsive (NR) to acoustic tones and bandpass noise. Crosses indicate neurons only tested with CI. B, CI best electrode maps show the same neurons as in A, with color corresponding to CI best electrode. Stimulation was between adjacent contacts in the electrode array, indicated by the pair of numbers on the y-axis. Symbols are the same as in A. Crosses indicate neurons only tested with acoustic stimulation. C, BF versus best electrode comparison of neurons from the left auditory cortex of one animal (M57U), contralateral to CI stimulation. Horizontal bars represent median BF values for each best electrode. The first column represents the BFs of CI-nonresponsive neurons. D, BF distributions for CI-driven and CI-nonresponsive neurons from all 4 animals

Temporal bone characterization and cochlear implant feasibility in the common marmoset (Callithrix jacchus)

(Johnson et al., 2012) This study reports the size of the marmoset scala tympani as it relates to the insertion of a multi-channel cochlear implant electrode. We also report a more complete set of measurements of marmoset temporal bone structures than has been reported previously. This includes characterization of cochlear fluid spaces, middle ear ossicles and semicircular canals. As the marmoset continues to be increasingly used as a model for auditory research, such measures will prove valuable for further comparative anatomy and modeling studies.

Fig. 7. Cochlear implant electrode insertion in an adult marmoset cochlea (M9R, 17 months). (a) A microCT image showing a 10 channel cochlear implant electrode (H12 Cochlear Ltd) that was inserted through a cochleostomy ∼1 mm apical to the round window. (b) 3-D reconstruction of the scala tympani and electrode overlaid with the microCT cross-section. The most apical band is inserted ∼8 mm, and electrodes are estimated to span a frequency-place range of 3–20 kHz. Frequency-place estimates were derived from the Greenwood function (Greenwood, 1990) scaled according to marmoset cochlear length and estimated audible frequency range (Osmanski and Wang, 2011). Electrode schematic was provided by Cochlear Ltd.