Distinct Manifestations of Cooperative, Multidimensional Stimulus Representations in Different Auditory Forebrain Stations.

Classic spectrotemporal receptive fields (STRFs) for auditory neurons are usually expressed as a single linear filter representing a single encoded stimulus feature. Multifilter STRF models represent the stimulus-response relationship of primary auditory cortex (A1) neurons more accurately because they can capture multiple stimulus features. To determine whether multifilter processing is unique to A1, we compared the utility of single-filter versus multifilter STRF models in the medial geniculate body (MGB), anterior auditory field (AAF), and A1 of ketamine-anesthetized cats. We estimated STRFs using both spike-triggered average (STA) and maximally informative dimension (MID) methods. Comparison of basic filter properties of first maximally informative dimension (MID1) and second maximally informative dimension (MID2) in the 3 stations revealed broader spectral integration of MID2s in MGBv and A1 as opposed to AAF. MID2 peak latency was substantially longer than for STAs and MID1s in all 3 stations. The 2-filter MID model captured more information and yielded better predictions in many neurons from all 3 areas but disproportionately more so in AAF and A1 compared with MGBv. Significantly, information-enhancing cooperation between the 2 MIDs was largely restricted to A1 neurons. This demonstrates significant differences in how these 3 forebrain stations process auditory information, as expressed in effective and synergistic multifilter processing.

Primary auditory cortical responses to electrical stimulation of the thalamus.

Cochlear implant electrical stimulation of the auditory system to rehabilitate deafness has been remarkably successful. Its deployment requires both an intact auditory nerve and a suitably patent cochlear lumen. When disease renders prerequisite conditions impassable, such as in neurofibromatosis type II and cochlear obliterans, alternative treatment targets are considered. Electrical stimulation of the cochlear nucleus and midbrain in humans has delivered encouraging clinical outcomes, buttressing the promise of central auditory prostheses to mitigate deafness in those who are not candidates for cochlear implantation. In this study we explored another possible implant target: the auditory thalamus. In anesthetized cats, we first presented pure tones to determine frequency preferences of thalamic and cortical sites. We then electrically stimulated tonotopically organized thalamic sites while recording from primary auditory cortical sites using a multichannel recording probe. Cathode-leading biphasic thalamic stimulation thresholds that evoked cortical responses were much lower than published accounts of cochlear and midbrain stimulation. Cortical activation dynamic ranges were similar to those reported for cochlear stimulation, but they were narrower than those found through midbrain stimulation. Our results imply that thalamic stimulation can activate auditory cortex at low electrical current levels and suggest an auditory thalamic implant may be a viable central auditory prosthesis.

Functional networks of parvalbumin-immunoreactive neurons in cat auditory cortex.

Inhibitory interneurons constitute ∼20% of auditory cortical cells and are essential for shaping sensory processing. Connectivity patterns of interneurons in relation to functional organization principles are not well understood. We contrasted the connection patterns of parvalbumin-immunoreactive cells in two functionally distinct cortical regions: the tonotopic, narrowly frequency-tuned module [central narrow band (cNB)] of cat central primary auditory cortex (AI) and the nontonotopic, broadly tuned second auditory field (AII). Interneuronal connectivity patterns and laminar distribution were identified by combining a retrograde tracer (wheat-germ agglutinin apo-horseradish peroxidase colloidal gold) with labeling of the Ca(2+) binding protein parvalbumin (Pv), a marker for the GABAergic interneurons usually described physiologically as fast-spiking neurons. In AI, parvalbumin-positive (Pv+) cells constituted 13% of the retrograde labeled cells in the immediate vicinity of the injection site, compared to 10% in AII. The retrograde labeling of Pv+ cells along isofrequency countours was confined to the cNB. The spatial spread of labeled excitatory neurons in AI was more than twice that found for Pv+ cells. By contrast, in the AII, the spread of Pv+ cells was nearly equal to that of excitatory neurons. The retrograde labeling of Pv+ cells was anisotropic in AI and isotropic in AII. This demonstration of inhibitory networks in auditory cortex reveals that the connections of cat GABAergic AI and AII cells follow different anatomical plans and thus contribute differently to the shaping of neural response properties. The finding that local connectivity of parvalbumin-immunoreactive neurons in AI is closely aligned with spectral integration properties demonstrates the critical role of inhibition in creating distinct processing modules in AI.

Improved stimulus representation by short interspike intervals in primary auditory cortex.

We analyzed the receptive field information conveyed by interspike intervals (ISIs) in the auditory cortex. In the visual system, different ISIs may both code for different visual features and convey differing amounts of stimulus information. To determine their potential role in auditory signal processing, we obtained extracellular recordings in the primary auditory cortex (AI) of the cat while presenting a dynamic moving ripple stimulus and then used the responses to construct spectrotemporal receptive fields (STRFs). For each neuron, we constructed three STRFs, one for short-ISI events (ISI < 15 ms); one for isolated, long-ISI events (ISI > 15 ms); and one including all events. To characterize stimulus encoding, we calculated the feature selectivity and event information for each of the STRFs. Short-ISI spikes were more feature selective and conveyed information more efficiently. The different ISI regimens of AI neurons did not represent different stimulus features, but short-ISI spike events did contribute over-proportionately to the full spike train STRF information. Thus short-ISIs constitute a robust representation of auditory features, and they are particularly effective at driving postsynaptic activity. This suggests that short-ISI events are especially suited to provide noise immunity and high-fidelity information transmission in AI.

Global hyper-synchronous spontaneous activity in the developing optic tectum.

Studies of patterned spontaneous activity can elucidate how the organization of neural circuits emerges. Using in vivo two-photon Ca(2+) imaging, we studied spatio-temporal patterns of spontaneous activity in the optic tectum of Xenopus tadpoles. We found rhythmic patterns of global synchronous spontaneous activity between neurons, which depends on visual experience and developmental stage. By contrast, synchronous spontaneous activity between non-neuronal cells is mediated more locally. To understand the source of the neuronal spontaneous activity, input to the tectum was systematically removed. Whereas removing input from the visual or mechanosensory system alone had little effect on patterned spontaneous activity, removing input from both systems drastically altered it. These results suggest that either input is sufficient to maintain the intrinsically generated spontaneous activity and that patterned spontaneous activity results from input from multisensory systems. Thus, the amphibian midbrain differs from the mammalian visual system, whose spontaneous activity is controlled by retinal waves.