Cortical Stimulation Induces Excitatory Postsynaptic Potentials of Inferior Colliculus Neurons in a Frequency-Specific Manner.

Corticofugal modulation of auditory responses in subcortical nuclei has been extensively studied whereas corticofugal synaptic transmission must still be characterized. This study examined postsynaptic potentials of the corticocollicular system, i.e., the projections from the primary auditory cortex (AI) to the central nucleus of the inferior colliculus (ICc) of the midbrain, in anesthetized C57 mice. We used focal electrical stimulation at the microampere level to activate the AI (ESAI) and in vivo whole-cell current-clamp to record the membrane potentials of ICc neurons. Following the whole-cell patch-clamp recording of 88 ICc neurons, 42 ICc neurons showed ESAI-evoked changes in the membrane potentials. We found that the ESAI induced inhibitory postsynaptic potentials in 6 out of 42 ICc neurons but only when the stimulus current was 96 µA or higher. In the remaining 36 ICc neurons, excitatory postsynaptic potentials (EPSPs) were induced at a much lower stimulus current. The 36 ICc neurons exhibiting EPSPs were categorized into physiologically matched neurons (n = 12) when the characteristic frequencies of the stimulated AI and recorded ICc neurons were similar (≤1 kHz) and unmatched neurons (n = 24) when they were different (>1 kHz). Compared to unmatched neurons, matched neurons exhibited a significantly lower threshold of evoking noticeable EPSP, greater EPSP amplitude, and shorter EPSP latency. Our data allow us to propose that corticocollicular synaptic transmission is primarily excitatory and that synaptic efficacy is dependent on the relationship of the frequency tunings between AI and ICc neurons.

The onset and post-onset auditory responses of cochlear nucleus neurons are modulated differently by cortical activation.

Auditory cortex exhibit a capacity of modulating the functions of subcortical auditory nuclei and even inner ear through descending pathways. The cochlear nucleus (CN), which acts as the gateway from the auditory periphery to the central auditory system, is also subjected to corticofugal modulation. Cortical modulation of subcortical nuclei is highly specific to the frequency tunings of cortical and subcortical neurons. It is unclear whether the high frequency-specificity of the cortical modulation of CN frequency tuning is implemented in the CN, in the auditory periphery, or in both. We analyzed the corticofugal effects on the frequency tuning, constructed from both onset (OS) and post-onset (pOS) response components of CN neurons in C57 mice. We found that the focal electrical stimulation of the primary auditory cortex (ESAI) induced remarkable changes in the response magnitude, response latency and the frequency response curves of CN neurons. The changes in the pOS components were highly specific to the difference in BFs between the stimulated AI neurons and recorded CN neurons. The changes in the OS component mostly involved the augmentation of the auditory responses of CN neurons, while exhibiting far poorer frequency-specificity. Considering the large differences in the temporal response patterns and the tuning shapes between the auditory nerve (AN) and the CN, our data suggest that the CN intrinsic neural circuitry plays a critical role in the frequency specificity of corticofugal modulation. Cortical modulation of the inner ear mostly contributes to the augmentation of the AN inputs to the CN, around the BFs of stimulated AI neurons.

Diversity of bilateral synaptic assemblies for binaural computation in midbrain single neurons.

Binaural hearing confers many beneficial functions but our understanding of its underlying neural substrates is limited. This study examines the bilateral synaptic assemblies and binaural computation (or integration) in the central nucleus of the inferior colliculus (ICc) of the auditory midbrain, a key convergent center. Using in-vivo whole-cell patch-clamp, the excitatory and inhibitory postsynaptic potentials (EPSPs/IPSPs) of single ICc neurons to contralateral, ipsilateral and bilateral stimulation were recorded. According to the contralateral and ipsilateral EPSP/IPSP, 7 types of bilateral synaptic assemblies were identified. These include EPSP-EPSP (EE), E-IPSP (EI), E-no response (EO), II, IE, IO and complex-mode (CM) neurons. The CM neurons showed frequency- and/or amplitude-dependent EPSPs/IPSPs to contralateral or ipsilateral stimulation. Bilateral stimulation induced EPSPs/IPSPs that could be larger than (facilitation), similar to (ineffectiveness) or smaller than (suppression) those induced by contralateral stimulation. Our findings have allowed our group to characterize novel neural circuitry for binaural computation in the midbrain.