Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil

Abstract

The neural representation of meaningful stimulus features is thought to rely on precise discharge characteristics of the auditory cortex. Precisely timed onset spikes putatively carry the majority of stimulus-related information in auditory cortical neurons but make a small contribution to stimulus representation in the auditory midbrain. Because these conclusions derive primarily from anesthetized preparations, we reexamined temporal coding properties of single neurons in the awake gerbil inferior colliculus (IC) and compared them with primary auditory cortex (AI). Surprisingly, AI neurons displayed a reduction of temporal precision compared with those in the IC. Furthermore, this hierarchical transition from high to low temporal fidelity was observed for both static and dynamic stimuli. Because most of the data that support temporal precision were obtained under anesthesia, we also reexamined response properties of IC and AI neurons under these conditions. Our results show that anesthesia has profound effects on the trial-to-trial variability and reliability of discharge and significantly improves the temporal precision of AI neurons to both tones and amplitude-modulated stimuli. In contrast, IC temporal properties are only mildly affected by anesthesia. These results underscore the pitfalls of using anesthetized preparations to study temporal coding. Our findings in awake animals reveal that AI neurons combine faster adaptation kinetics and a longer temporal window than evident in IC to represent ongoing acoustic stimuli.

Processing Temporal Modulations in Binaural and Monaural Auditory Stimuli by Neurons in the Inferior Colliculus and Auditory Cortex

“…Using AM electrical pulse trains delivered to cochlear implants, Middlebrooks (2008) showed an inverse relationship between AM group delays and cutoff frequencies in cortical neurons. Although our observation of the cutoff frequencies for neurons to monaural AM tones in the IC (158 Hz) are similar to those in unanesthetized gerbil (190 Hz;Ter-Mikaelian et al 2007), our cutoffs for cortical neurons to the same stimuli are considerably higher (26 Hz) than those in the gerbil (7 Hz). The reason for this difference is not clear.…”

“…Ter-Mikaelian et al (2007) showed that anesthesia altered the variability and the temporal precision of auditory cortical neurons to AM tones. In contrast, neurons in the IC were found to be less affected by anesthesia.…”

Age-Related Changes in the Relationship Between Auditory Brainstem Responses and Envelope-Following Responses

“…Then the animals were removed from anesthesia, and an intramuscular injection of dexmedetomidine (Dexdomitor, 0.1-0.2 mg/kg) was administered. Dexmedetomidine is an α-adrenergic agonist that acts as an analgesic and a sedative and is known to not affect auditory responses in the midbrain (Ter-Mikaelian et al 2007). This maintains the animals in an unanesthetized condition, where they still respond to pain stimuli, like a foot pinch, but are otherwise immobile and amenable for 2 to 3-h recording sessions.…”

Millisecond encoding precision of auditory cortex neurons

“…Together, these results may be taken to suggest that millisecond-precise spike timing of individual auditory cortex neurons may not encode additional information about complex sounds beyond that contained in the spike rate on the 10-to 20-ms scale. However, it could also be that the importance of precisely stimulus-locked spike patterns was masked in previous studies, because anesthetic drugs can suppress stimulus-synchronized spikes (12,13), because stimulus-induced temporal patterns of cortical activity may be less precise during the presentation of brief artificial sounds than during the presentation of extended periods of naturalistic sounds (14,15), or because some previously used analysis methods did not capture all possible information carried by the responses (16).…”