Enhancement and distortion in the temporal representation of sounds in the ventral cochlear nucleus of chinchillas and cats.

A subset of neurons in the cochlear nucleus (CN) of the auditory brainstem has the ability to enhance the auditory nerve's temporal representation of stimulating sounds. These neurons reside in the ventral region of the CN (VCN) and are usually known as highly synchronized, or high-sync, neurons. Most published reports about the existence and properties of high-sync neurons are based on recordings performed on a VCN output tract--not the VCN itself--of cats. In other species, comprehensive studies detailing the properties of high-sync neurons, or even acknowledging their existence, are missing.Examination of the responses of a population of VCN neurons in chinchillas revealed that a subset of those neurons have temporal properties similar to high-sync neurons in the cat. Phase locking and entrainment--the ability of a neuron to fire action potentials at a certain stimulus phase and at almost every stimulus period, respectively--have similar maximum values in cats and chinchillas. Ranges of characteristic frequencies for high-sync neurons in chinchillas and cats extend up to 600 and 1000 Hz, respectively. Enhancement of temporal processing relative to auditory nerve fibers (ANFs), which has been shown previously in cats using tonal and white-noise stimuli, is also demonstrated here in the responses of VCN neurons to synthetic and spoken vowel sounds.Along with the large amount of phase locking displayed by some VCN neurons there occurs a deterioration in the spectral representation of the stimuli (tones or vowels). High-sync neurons exhibit a greater distortion in their responses to tones or vowels than do other types of VCN neurons and auditory nerve fibers.Standard deviations of first-spike latency measured in responses of high-sync neurons are lower than similar values measured in ANFs' responses. This might indicate a role of high-sync neurons in other tasks beyond sound localization

Temporal and spectral analyses of responses to /ε/ of high-sync and Group 3 VCN neurons.

<p>Panels A–C display period histograms obtained from responses of three high-sync neurons whose CF is indicated in each panel. Panel A recordings originate from the ventral acoustic stria. Panels G–I contain period histograms computed from responses of three VCN neurons (Group 3; CF indicated in each panel). Panels D–F (black continuous lines) and J–L (black continuous lines) show result of Fourier analysis obtained from responses shown in panels A–C and G–I, respectively. Dashed lines in panels J–L illustrate PSDs from three other VCN neurons (Group 3; CF indicated in each panel).</p

Normalized SACs and harmonic distortion of VCN neurons' responses to /ε/.

<p>Panels in A, C and E contain normalized SACs constructed from high-sync neurons (thin lines) and Group 3 neurons (red thick lines) responses to /ε/. High-sync neurons in A, C and E are the same neurons whose histograms are shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044286#pone-0044286-g010" target="_blank">Figs. 10A–10C</a>, respectively. Group 3 neurons in panel A, C and E are the same as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044286#pone-0044286-g010" target="_blank">Figs. 10–10C</a>. Panel B displays a scatter plot of CIs as a function of CF for high-sync (filled triangles, N = 13), Group 2 (open triangles, N = 6) and Group 3 VCN neurons (inverted triangles, N = 13). Panel C displays THDs for the same neurons in panel B.</p

Distortion as a function of synchrony and interspike interval variability.

<p>Black filled (N = 26 and 34 in chinchillas and cats, respectively) and open “up” triangles (N = 16 and 2 in chinchillas and cats, respectively) represent data from high-sync and Group 2 VCN neurons, respectively. “Down” triangles represent data from Group 3 VCN neurons (N = 18). Red dots show cat ANF data (N = 59). Data from chinchillas are in panels A and B, and from cats in panels C and D.</p

Temporal processing of the whispered /<i>i</i>/ vowel by high-sync neurons and ANFs.

<p>Panels A and B, respectively, display amplitudes and bandwidths of the central peaks in SACs computed from responses of cat high-sync neurons (black triangles, N = 19) and ANFs (red dots, N = 24) to the whispered /<i>i</i>/ sound. The results of the distortion analysis performed on the responses of high-sync neurons and ANFs are shown in panel C.</p

Single tone responses of two cat high-sync neurons.

<p>Data from two cat VCN neurons shown in a similar fashion to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044286#pone-0044286-g002" target="_blank">Fig. 2</a>. Stimulus frequency used to evoke data in panels A and B are 400 and 900 Hz, respectively. Firing rates, except for those indicated by the red dashed lines, were measured during the stimulus duration (0–50 ms). Red dashed lines represent onset firing rates evoked by 90-dB tones, except in panel F (70 dB SPL).</p

PSD and dominant-component analyses of SACs.

<p>Panels A and B show Fourier transform amplitude of SACs displayed on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044286#pone-0044286-g012" target="_blank">Figs. 12C and 12 E</a>, respectively, using the same color convention. Panel C exhibits a scatter plot of the frequencies of dominant components as a function of CF for a population of high-sync neurons (N = 19) and ANFs (N = 24).</p

Responses to synthetic vowel sounds.

<p>Panels A and C exhibit period histograms obtained from ANF responses to the /<i>i</i>/ sound. Responses of two high-sync neurons to the same stimulus are shown in panels B and D. <i>r</i> values indicate strength of phase locking to <i>f</i>₀ ( = 100 Hz). Panels E and F contrast SACs computed from high-sync neurons' (thin lines) and ANFs' (red thick lines) responses to /<i>i</i>/. Spike trains used to compute SACs in panel D are the ones used in panels A and B. Similarly, SACs in E and F were computed from response whose histograms appear in panels C and D.</p

Responses of high-sync neurons and ANFs to the whispered /<i>i</i>/ sound.

<p>Panel A display the result of the PSD analysis of the whispered <b>/</b><i>i</i><b>/</b> vowel. F₁, F₂ and F₃ represent the approximate location of the respective formants. Panels B and D show dot raster plots of the responses of a high-sync neuron and an ANF, respectively. SACs obtained from responses in B and C are shown in panel C (thin line: high-sync neuron; red thick line: ANF). SACs in panel E were obtained from data from another high-sync/ANF pair, with same CF ( = 900 Hz).</p

Response properties of PLN/OL neurons in chinchilla.

<p>Data across rows come from the same neuron. Left column (i.e., panels A, D, G and J) shows response area curves for four VCN neurons. Center column exhibits response area curves using vector strength values as a response metric. Right column displays PSTHs obtained from responses to CF tones. Standard deviations of first-spike latencies (σ_FSL) are next to each PSTH.</p