Enhancement and Distortion in the Temporal Representation of Sounds in the Ventral Cochlear Nucleus of Chinchillas and Cats Alberto Recio-Spinoso* Laboratory for Auditory Neuroengineering, IDINE, Universidad de Castilla-La Mancha, Albacete, Spain Abstract 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. Citation: Recio-Spinoso A (2012) Enhancement and Distortion in the Temporal Representation of Sounds in the Ventral Cochlear Nucleus of Chinchillas and Cats. PLoS ONE 7(9): e44286. doi:10.1371/journal.pone.0044286 Editor: Manuel S. Malmierca, University of Salamanca - Institute for Neuroscience of Castille and Leon and Medical School, Spain Received March 26, 2012; Accepted August 1, 2012; Published September 18, 2012 Copyright: 2012 Alberto Recio-Spinoso. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Work was supported by National Institute on Deafness and Other Communication Disorders grant NS-17590 (http://www.nidcd.nih.gov) and by the Regional Operational Programme European Social Fund 2007/2013 within the frame of the Spain Instituto de Recursos Humanos para la Ciencia y la Tecnolog´ıa program of the Fundacio´ n Parque Cient´ıfico y Tecnolo´ gico de Albacete (http://www.pcyta.com). The funding agencies had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The author has declared that no competing interests exist. * E-mail: alberto.recio@uclm.es Introduction In response to low-frequency sinusoidal sounds, auditory nerve fibers (ANFs) generate trains of action potentials, or spikes, that are synchronized to the stimulating waveform—a property usually known as phase locking [1,2]. Temporal processing is a key function of the auditory system, as it is relevant for the detection of features important for speech comprehension [3]. Quantification of phase locking is usually done using the vector strength (r) metric [4], where 0#r#1. (A value of r = 1 indicates perfect synchronization to one phase of the stimulus waveform; r = 0 implies a lack of preference to any particular stimulus phase.) In cat, maximum r values, rmax, hold relatively constant for stimulus frequencies below 1 kHz and decrease gradually up to around 5 kHz [5,6]. Responses to characteristic frequency (CF: frequency of lowest threshold) tones by cat ANFs yield rmax#0.9 [5,6,7,8]. In chinchilla, ANF responses to CF tones also produce rmax#0.9 [9,10]. Phase locking is also a property of neurons in the cochlear nucleus (CN)—the brainstem structure to which ANFs project. Different CN regions exhibit different amounts of phase locking [11,12], with neurons in the ventral portion of the CN (VCN) being more adept at temporal processing than those in the dorsal CN. A discrepancy exists, however, among published studies regarding synchronization limits of VCN neurons with CFs below approximately 1 kHz. Some studies have found that phase-locking strength exhibited by VCN neurons deteriorates or remains constant relative to ANFs [11,13–16]. The work of others [6,7,17,18], however, has shown an enhancement in phase locking relative to the auditory nerve (AN), at least for CFs below 1 kHz. AVCN neurons in cat that show an improvement in phase locking over auditory nerve fibers often exhibit rmax.0.9 in their responses to CF tones—greater than rmax values computed from ANF responses to CF tones. These neurons, which are usually referred to as highly synchronized (or high-sync), are also capable of firing action potentials at almost every stimulus cycle, a property called entrainment [6,19,20]. Variability in interspike intervals, such as in ANF’s spike trains, yields lower entrainment levels while increasing the quality of the stimulus waveform representation [20,21]. Temporal processing enhancement in the VCN seems less prominent in rodents than in cats [19]. Moreover, published works PLOS ONE | www.plosone.org 1 September 2012 | Volume 7 | Issue 9 | e44286