Behavioral training restores temporal processing in auditory cortex of long-deaf cats

Abstract

Temporal auditory processing is poor in prelingually hearing-impaired patients fitted with cochlear prostheses as adults. In an animal model of prelingual long-term deafness, we investigated the effects of behavioral training on temporal processing in the adult primary auditory cortex (AI). Neuronal responses to pulse trains of increasing frequencies were recorded in three groups of neonatally deafened cats that received a cochlear prosthesis after >3 yr of deafness: 1) acutely implanted animals that received no electric stimulation before study, 2) animals that received chronic-passive stimulation for several weeks to months before study, and 3) animals that received chronic-passive stimulation and additional behavioral training (signal detection). A fourth group of normal adult cats that was deafened acutely and implanted served as controls. The neuronal temporal response parameters of interest included the stimulus rate that evoked the maximum number of phase-locked spikes [best repetition rate (BRR)], the stimulus rate that produced 50% of the spike count at BRR (cutoff rate), the peak-response latency, and the first spike latency and timing-jitter. All long-deaf animals demonstrated a severe reduction in spiral ganglion cell density (mean, <6% of normal). Long-term deafness resulted in a significantly reduced temporal following capacity and spike-timing precision of cortical neurons in all parameters tested. Neurons in deaf animals that received only chronic-passive stimulation showed a gain in BRR but otherwise were similar to deaf cats that received no stimulation. In contrast, training with behaviorally relevant stimulation significantly enhanced all temporal processing parameters to normal levels with the exception of minimum latencies. These results demonstrate the high efficacy of learning-based remodeling of fundamental timing properties in cortical processing even in the adult, long-deaf auditory system, suggesting rehabilitative strategies for patients with long-term hearing loss.

Direct Recordings from the Auditory Cortex in a Cochlear Implant User

“…Thus, direct comparison of animal studies done in congenitally or neonatally deaf animals with our present findings obtained in a postlingually deaf patient with a long (and successful) history of CI use is not straightforward. We note, however, that chronic electrical stimulation of the auditory nerve, particularly when coupled with behavioral training, can improve temporal processing within the primary auditory cortex of experimentally deafened animals Vollmer and Beitel 2011). The present report is consistent with these animal electrophysiology studies and extends their findings to human nonprimary auditory cortex.…”

Pairing Speech Sounds With Vagus Nerve Stimulation Drives Stimulus-specific Cortical Plasticity

“…These individuals require extensive interventions in order to improve speech perception and cortical responses to sounds [16–19,47]. For example, auditory cortex responses are slow and weak in deaf individuals [48,49].…”

“…Many studies have demonstrated that language impaired individuals have weak auditory cortex responses to sound that can be strengthened following extensive rehabilitation therapy [16–19]. Vagus nerve stimulation is a safe, well-tolerated procedure that is frequently used to treat patients with epilepsy or depression [20–22].…”

Behavioral frequency discrimination ability of partially deafened cats using cochlear implants

“…There have been multiple studies which assessed ICES in animal behavioral models (Vollmer et al, 2001, Vollmer and Beitel, 2011, Kral et al, 2006, Klinke et al, 1999, Beitel et al, 2000). However, results from these studies are not comparable with results from the present experiment due to: 1) effects of electrical stimulation differ significantly between partially and profoundly deaf cochlea (Von Ilberg et al, 2011); 2) none of the above studies used a partial hearing, ICES behavioral model; and 3) conditioning and detection tasks are different from discrimination tasks in terms of their objectives.…”

“…While other studies have used conditioning to provide animals with behaviorally relevant auditory experience (Kral et al, 2006, Klinke et al, 1999), these studies did not allow performance to be measured. Others have used avoidance conditioning to train cats to detect stimulation thresholds (Vollmer et al, 2001, Beitel et al, 2000, Vollmer and Beitel, 2011) and discriminate changes in modulation frequency (Vollmer et al, 2001). In those experiments individual electrodes were tested one at a time and subjects received only electric but not acoustic stimulation.…”