Exploring the Structural and Functional Organization of the Dorsal Zone of Auditory Cortex in Hearing and Deafness

Recent neuroscientific research has focused on cortical plasticity, which refers to the ability of the cerebral cortex to adapt as a consequence of experience. Over the past decade, an increasing number of studies have convincingly shown that the brain can adapt to the loss or impairment of a sensory system, resulting in the expansion or heightened ability of the remaining senses. A particular region in cat auditory cortex, the dorsal zone (DZ), has been shown to mediate enhanced visual motion detection in deaf animals. The purpose of this thesis is to further our understanding of the structure and function of DZ in both hearing and deaf animals, in order to better understand how the brain compensates following insult or injury to a sensory system, with the ultimate goal of improving the utility of sensory prostheses. First, I demonstrate that the brain connectivity profile of animals with early- and late-onset deafness is similar to that of hearing animals, but the projection strength to visual brain regions involved in motion processing increases as a consequence of deafness. Second, I specifically evaluate the functional impact of the strongest auditory connections to area DZ using reversible deactivation and electrophysiological recordings. I show that projections that ultimately originate in primary auditory cortex (A1) form much of the basis of the response of DZ neurons to auditory stimulation. Third, I show that almost half of the neurons in DZ are influenced by visual or somatosensory information. I further demonstrate that this modulation by other sensory systems can have effects that are opposite in direction during different portions of the auditory response. I also show that techniques that incorporate the responses of multiple neurons, such as multi-unit and local field potential recordings, may vastly overestimate the degree to which multisensory processing occurs in a given brain region. Finally, I confirm that individual neurons in DZ become responsive mainly to visual stimulation following deafness. Together, these results shed light on the function and structural organization of area DZ in both hearing and deaf animals, and will contribute to the development of a comprehensive model of cross-modal plasticity

Ubiquitous Crossmodal Stochastic Resonance in Humans: Auditory Noise Facilitates Tactile, Visual and Proprioceptive Sensations

BACKGROUND: Stochastic resonance is a nonlinear phenomenon whereby the addition of noise can improve the detection of weak stimuli. An optimal amount of added noise results in the maximum enhancement, whereas further increases in noise intensity only degrade detection or information content. The phenomenon does not occur in linear systems, where the addition of noise to either the system or the stimulus only degrades the signal quality. Stochastic Resonance (SR) has been extensively studied in different physical systems. It has been extended to human sensory systems where it can be classified as unimodal, central, behavioral and recently crossmodal. However what has not been explored is the extension of this crossmodal SR in humans. For instance, if under the same auditory noise conditions the crossmodal SR persists among different sensory systems. METHODOLOGY/PRINCIPAL FINDINGS: Using physiological and psychophysical techniques we demonstrate that the same auditory noise can enhance the sensitivity of tactile, visual and propioceptive system responses to weak signals. Specifically, we show that the effective auditory noise significantly increased tactile sensations of the finger, decreased luminance and contrast visual thresholds and significantly changed EMG recordings of the leg muscles during posture maintenance. CONCLUSIONS/SIGNIFICANCE: We conclude that crossmodal SR is a ubiquitous phenomenon in humans that can be interpreted within an energy and frequency model of multisensory neurons spontaneous activity. Initially the energy and frequency content of the multisensory neurons' activity (supplied by the weak signals) is not enough to be detected but when the auditory noise enters the brain, it generates a general activation among multisensory neurons of different regions, modifying their original activity. The result is an integrated activation that promotes sensitivity transitions and the signals are then perceived. A physiologically plausible model for crossmodal stochastic resonance is presented

Multisensory responses in primary auditory cortex of the cat

Core auditory cortex of the cat is comprised of primary auditory cortex (A1) and the anterior auditory field (AAF). Neurons in both fields respond strongly to acoustic stimuli and are tonotopically organized. In hearing animals, a small number of cells in AAF respond to tactile stimulation. However, it is unclear if multisensory input influences responses in A1. In this study, multisensory stimuli were developed by pairing a pure tone stimulus with a flash stimulus at various stimulus onset asynchronies. A linear multielectrode array recorded multi-unit activity in A1 across cortical layers. We identified unisensory auditory, unisensory visual, bimodal, and subthreshold multisensory multi-unit activity. We also found neurons where auditory-visual interactions either suppressed or enhanced neuronal activity. Additionally, visual stimulation can modulate the neural response to auditory inputs depending on the stimulus onset asynchrony. Taken together, the majority of neural activity in A1 in the cat is influenced by visual inputs

Predictive coding and stochastic resonance as fundamental principles of auditory phantom perception

Mechanistic insight is achieved only when experiments are employed to test formal or computational models. Furthermore, in analogy to lesion studies, phantom perception may serve as a vehicle to understand the fundamental processing principles underlying healthy auditory perception. With a special focus on tinnitus—as the prime example of auditory phantom perception—we review recent work at the intersection of artificial intelligence, psychology and neuroscience. In particular, we discuss why everyone with tinnitus suffers from (at least hidden) hearing loss, but not everyone with hearing loss suffers from tinnitus. We argue that intrinsic neural noise is generated and amplified along the auditory pathway as a compensatory mechanism to restore normal hearing based on adaptive stochastic resonance. The neural noise increase can then be misinterpreted as auditory input and perceived as tinnitus. This mechanism can be formalized in the Bayesian brain framework, where the percept (posterior) assimilates a prior prediction (brain’s expectations) and likelihood (bottom-up neural signal). A higher mean and lower variance (i.e. enhanced precision) of the likelihood shifts the posterior, evincing a misinterpretation of sensory evidence, which may be further confounded by plastic changes in the brain that underwrite prior predictions. Hence, two fundamental processing principles provide the most explanatory power for the emergence of auditory phantom perceptions: predictive coding as a top-down and adaptive stochastic resonance as a complementary bottom-up mechanism. We conclude that both principles also play a crucial role in healthy auditory perception. Finally, in the context of neuroscience-inspired artificial intelligence, both processing principles may serve to improve contemporary machine learning techniques

Identification of Persistent and Resurgent Sodium Currents in Spiral Ganglion Neurons Cultured from the Mouse Cochlea

In spiral ganglion neurons (SGNs), the afferent single units of the auditory nerve, high spontaneous and evoked firing rates ensure preservation of the temporal code describing the key features of incoming sound. During postnatal development, the spatiotemporal distribution of ion channel subtypes contributes to the maturation of action potential generation in SGNs, and to their ability to generate spike patterns that follow rapidly changing inputs. Here we describe tetrodotoxin (TTX)-sensitive Na+ currents in SGNs cultured from mice, whose properties may support this fast spiking behavior. A subthreshold persistent Na+ current (INaP) and a resurgent Na+ current (INaR) both emerged prior to the onset of hearing and became more prevalent as hearing matured. Navβ4 subunits, which are proposed to play a key role in mediating INaR elsewhere in the nervous system, were immunolocalized to the first heminode where spikes are generated in the auditory nerve, and to perisomatic nodes of Ranvier. ATX-II, a sea anemone toxin that slows classical Na+ channel inactivation selectively, enhanced INaP five-fold and INaR three-fold in voltage clamp recordings. In rapidly-adapting SGNs under current clamp, ATX-II increased the likelihood of firing additional action potentials. The data identify INaP and INaR as novel regulators of excitability in SGNs, and consistent with their roles in other neuronal types, we suggest that these nonclassical Na+ currents may contribute to the control of refractoriness in the auditory nerve

Visuo-auditory interactions in the primary visual cortex of the behaving monkey: Electrophysiological evidence

<p>Abstract</p> <p>Background</p> <p>Visual, tactile and auditory information is processed from the periphery to the cortical level through separate channels that target primary sensory cortices, from which it is further distributed to functionally specialized areas. Multisensory integration is classically assigned to higher hierarchical cortical areas, but there is growing electrophysiological evidence in man and monkey of multimodal interactions in areas thought to be unimodal, interactions that can occur at very short latencies. Such fast timing of multisensory interactions rules out the possibility of an origin in the polymodal areas mediated through back projections, but is rather in favor of heteromodal connections such as the direct projections observed in the monkey, from auditory areas (including the primary auditory cortex AI) directly to the primary visual cortex V1. Based on the existence of such AI to V1 projections, we looked for modulation of neuronal visual responses in V1 by an auditory stimulus in the awake behaving monkey.</p> <p>Results</p> <p>Behavioral or electrophysiological data were obtained from two behaving monkeys. One monkey was trained to maintain a passive central fixation while a peripheral visual (V) or visuo-auditory (AV) stimulus was presented. From a population of 45 V1 neurons, there was no difference in the mean latencies or strength of visual responses when comparing V and AV conditions. In a second active task, the monkey was required to orient his gaze toward the visual or visuo-auditory stimulus. From a population of 49 cells recorded during this saccadic task, we observed a significant reduction in response latencies in the visuo-auditory condition compared to the visual condition (mean 61.0 vs. 64.5 ms) only when the visual stimulus was at midlevel contrast. No effect was observed at high contrast.</p> <p>Conclusion</p> <p>Our data show that single neurons from a primary sensory cortex such as V1 can integrate sensory information of a different modality, a result that argues against a strict hierarchical model of multisensory integration. Multisensory interaction in V1 is, in our experiment, expressed by a significant reduction in visual response latencies specifically in suboptimal conditions and depending on the task demand. This suggests that neuronal mechanisms of multisensory integration are specific and adapted to the perceptual features of behavior.</p