Changes in the Response Properties of Inferior Colliculus Neurons Relating to Tinnitus

Abstract

Tinnitus is often identified in animal models by using the gap prepulse inhibition of acoustic startle. Impaired gap detection following acoustic over-exposure (AOE) is thought to be caused by tinnitus “filling in” the gap, thus, reducing its salience. This presumably involves altered perception, and could conceivably be caused by changes at the level of the neocortex, i.e., cortical reorganization. Alternatively, reduced gap detection ability might reflect poorer temporal processing in the brainstem, caused by AOE; in which case, impaired gap detection would not be a reliable indicator of tinnitus. We tested the latter hypothesis by examining gap detection in inferior colliculus (IC) neurons following AOE. Seven of nine unilaterally noise-exposed guinea pigs exhibited behavioral evidence of tinnitus. In these tinnitus animals, neural gap detection thresholds (GDTs) in the IC significantly increased in response to broadband noise stimuli, but not to pure tones or narrow-band noise. In addition, when IC neurons were sub-divided according to temporal response profile (onset vs. sustained firing patterns), we found a significant increase in the proportion of onset-type responses after AOE. Importantly, however, GDTs were still considerably shorter than gap durations commonly used in objective behavioral tests for tinnitus. These data indicate that the neural changes observed in the IC are insufficient to explain deficits in behavioral gap detection that are commonly attributed to tinnitus. The subtle changes in IC neuron response profiles following AOE warrant further investigation.

Reductions in cortical alpha activity, enhancements in neural responses and impaired gap detection caused by sodium salicylate in awake guinea pigs

“…Here, we found that there were some increases in neural gap detection thresholds (in response to BBN) 2 h following sodium salicylate administration. This was consistent with the results of Berger et al (2014) in the inferior colliculus following noise exposure, as well as Deng et al (2010), who demonstrated increases in auditory cortex MGDTs following salicylate administration in rats. However, there was only one GP with minimum neural gap detection thresholds of greater than 50 ms, thereby suggesting that, for the majority of GPs, their temporal acuity was not affected to an extent that they would no longer be able to perform the behavioural task.…”

“…This was consistent with the results of Berger et al . () in the inferior colliculus following noise exposure, as well as Deng et al . (), who demonstrated increases in auditory cortex MGDTs following salicylate administration in rats.…”

“…Baseline PPI of the Preyer reflex was measured in each GP over a 2‐week period (minimum of three and a maximum of six testing sessions). Startling stimuli (BBN bursts of 20 ms; rise/fall time of 1 ms) and continuous background noise conditions (either BBN or 2 kHz wide narrow‐band noise centred at 5, 9, 13 or 17 kHz) were used, as described previously (Berger et al ., , ; Coomber et al ., ). A gap duration of 50 ms was used to elicit gap‐induced PPI, consistent with that used by others (e.g.…”

“…Neural gap detection thresholds were determined using the method described in Berger et al (2014). Briefly, auditory stimuli comprised a broadband noise (BBN) burst (duration of 200 ms, on/off ramps of 0.5 ms), followed by a fixed-length period of silence or 'gap' (durations of either 1, 2, 4, 8, 10, 20, 50 or 75 ms) and a final BBN burst (duration of 50 ms, on/off ramps of 2 ms), all presented at 70 dB SPL.…”

“…Moreover, by employing a GPIAS paradigm, Fournier & Hebert () were able to demonstrate significant deficits in gap detection in tinnitus patients, albeit at frequencies below their tinnitus. Indeed, work from our own laboratory indicated that minimum gap detection thresholds (MGDTs) in the inferior colliculus were slightly increased following noise exposure, but not to an extent that could explain behavioural gap detection deficits that were present in the same animals (Berger et al ., ).…”