Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus

Abstract

Auditory neurons that exhibit stimulus-specific adaptation (SSA) decrease their response to common tones while retaining responsiveness to rare ones. We recorded single-unit responses from the inferior colliculus (IC) where SSA is known to occur and we explored for the first time SSA in the cochlear nucleus (CN) of rats. We assessed an important functional outcome of SSA, the extent to which frequency discriminability depends on sensory context. For this purpose, pure tones were presented in an oddball sequence as standard (high probability of occurrence) or deviant (low probability of occurrence) stimuli. To study frequency discriminability under different probability contexts, we varied the probability of occurrence and the frequency separation between tones. The neuronal sensitivity was estimated in terms of spike-count probability using signal detection theory. We reproduced the finding that many neurons in the IC exhibited SSA, but we did not observe significant SSA in our CN sample. We concluded that strong SSA is not a ubiquitous phenomenon in the CN. As predicted, frequency discriminability was enhanced in IC when stimuli were presented in an oddball context, and this enhancement was correlated with the degree of SSA shown by the neurons. In contrast, frequency discrimination by CN neurons was independent of stimulus context. Our results demonstrated that SSA is not widespread along the entire auditory pathway, and suggest that SSA increases frequency discriminability of single neurons beyond that expected from their tuning curves.

Modulation of stimulus‐specific adaptation by GABAA receptor activation or blockade in the medial geniculate body of the anaesthetized rat

“…The existence of consecutive gain controls over SSA in diverse auditory nuclei (IC and MGB, so far) suggests the existence of successive hierarchical levels of processing through the auditory system that would allow the reduction of redundant information. If SSA is generated in the IC (Malmierca et al ; Ayala & Malmierca, ; Ayala et al ), the first important GABAergic modulation will occur at this lowest level and will require additional adjustments as SSA is propagated up the auditory pathway through the MGB. The rat MGB contains one‐fifth of the number of neurons present in the IC (Kulesza et al ).…”

“…Each frequency in the pair was always presented at the same sound level. Stimuli presented in an oddball paradigm were similar to those used to record mismatch negativity responses in human (Näätänen, ) and SSA responses in animal (Ulanovsky et al , ; Malmierca et al ; Antunes et al ; Duque et al ; Ayala et al ; Richardson et al ) studies. Briefly, 300 stimuli containing both frequencies were presented in a probabilistic manner: one frequency ( f 1 ) presented as a standard sound (90% of occurrence) was interspersed randomly with a second deviant (10% of occurrence) stimulus frequency ( f 2 ).…”

Auditory System

“…Ma et al (2002) have shown a role for presynaptic GABA B receptors. Studies using microiontophoresis in vivo have demonstrated that both GABA and glycine inhibit IC neurons in several species (LeBeau et al, 1996;Palombi and Caspary, 1996a;Vaughn et al, 1996), including rat (Faingold et al, 1989(Faingold et al, , 1991Pérez-Gonzalez et al, 2012;Pérez-Gonzalez and Malmierca, 2012). Rat IC neurons also possess NMDA and AMPA receptors (Petralia and Wenthold, 1992;Ishii et al, 1993;Petralia et al, 1994;Gaza and Ribak, 1997;Caicedo and Eybalin, 1999;Schmid et al, 2001).…”

Stimulus-specific adaptation and deviance detection in the inferior colliculus

“…In the brainstem, SSA has been recently explored in the ventral and dorsal cochlear nucleus of the rat and the results suggest that all cochlear nucleus neurons tested lack SSA (Ayala et al, 2012). Thus, the IC is the earliest center where SSA has been described (Malmierca et al, 2009a), although it remains to be tested whether or not other brainstem nuclei located in between the cochlear nucleus and IC show some degree of SSA.…”