Silencing cortical activity during sound-localization training impairs auditory perceptual learning

The brain has a remarkable capacity to adapt to changes in sensory inputs and to learn from experience. However, the neural circuits responsible for this flexible processing remain poorly understood. Using optogenetic silencing of ArchT-expressing neurons in adult ferrets, we show that within-trial activity in primary auditory cortex (A1) is required for training-dependent recovery in sound-localization accuracy following monaural deprivation. Because localization accuracy under normal-hearing conditions was unaffected, this highlights a specific role for cortical activity in learning. A1-dependent plasticity appears to leave a memory trace that can be retrieved, facilitating adaptation during a second period of monaural deprivation. However, in ferrets in which learning was initially disrupted by perturbing A1 activity, subsequent optogenetic suppression during training no longer affected localization accuracy when one ear was occluded. After the initial learning phase, the reweighting of spatial cues that primarily underpins this plasticity may therefore occur in A1 target neurons

Relationship between PPI and baseline startle response

Prepulse inhibition (PPI) of the startle response to a sudden noise is the reduction in startle observed when the noise is preceded shortly by a mild sensory event, which is often a tone. A part of the literature is based on the assumption that PPI is independent of the baseline startle. A simple model is presented and experimental validation provided. The model is based on the commonly accepted observation that the neuronal circuit of PPI differs from that of startle. But, by using a common output, the measures of both phenomena become linked to each other. But, how can we interpret the numerous experimental data showing PPI to be independent of the startle level? It is suggested that in a number of such cases the baseline startle would have been stabilized by a ceiling effect in the startle/PPI neuronal networks. Reducing the startle level, for example in a PPI evaluation procedure, may disclose properties of startle masked by this ceiling effect. Disclosure of habituation to the startle eliciting noise produced an increase of PPI along its initial measurements. Taken together, even if the neuronal process that sustains startle and PPI are distinct, separating them experimentally requires careful parametric methods and caution in the interpretation of the corresponding observations

Egocentric and allocentric representations in auditory cortex

A key function of the brain is to provide a stable representation of an object’s location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position

Effect of Audiovisual Training on Monaural Spatial Hearing in Horizontal Plane

The article aims to test the hypothesis that audiovisual integration can improve spatial hearing in monaural conditions when interaural difference cues are not available. We trained one group of subjects with an audiovisual task, where a flash was presented in parallel with the sound and another group in an auditory task, where only sound from different spatial locations was presented. To check whether the observed audiovisual effect was similar to feedback, the third group was trained using the visual feedback paradigm. Training sessions were administered once per day, for 5 days. The performance level in each group was compared for auditory only stimulation on the first and the last day of practice. Improvement after audiovisual training was several times higher than after auditory practice. The group trained with visual feedback demonstrated a different effect of training with the improvement smaller than the group with audiovisual training. We conclude that cross-modal facilitation is highly important to improve spatial hearing in monaural conditions and may be applied to the rehabilitation of patients with unilateral deafness and after unilateral cochlear implantation

Direct input from cochlear root neurons to pontine reticulospinal neurons in albino rat.

The cochlear root neurons (CRNs) are thought to mediate the auditory startle reflex (ASR) in the rat, which is widely used as a behavioral model for the investigation of the sensorimotor integration. CRNs project, among other targets, to the nucleus reticularis pontis caudalis (PnC), a major component of the ASR circuit, but little is known about the organization of this projection. Thus, we injected biotinylated dextran amine (BDA) in CRNs to study their projections with light and electron microscopy. Also, we performed double-labeling experiments, injecting BDA in the CRNs and subunit B of the cholera toxin or Fluorogold in the spinal cord to verify that CRNs project onto reticulospinal neurons. Electron microscopy of the labeled CRNs axons and terminals showed that even their most central and thinnest processes are myelinated. Most of the terminals are axodendritic, with multiple asymmetric synapses, and contain round vesicles (50 nm diameter). Double-labeling experiments demonstrated that CRN terminals are apposed to retrogradely labeled reticulospinal neurons in the contralateral nucleus reticularis PnC and bilaterally in the lateral paragigantocellular nucleus. Analyses of serial sections revealed that multiple CRNs synapse on single reticulospinal neurons in PnC, suggesting a convergence of auditory information. The morphometric features of these neurons classify them as giant neurons. This study confirms that CRNs project directly onto reticulospinal neurons and presents other anatomical features of the CRNs that contribute to a better understanding of the circuitry of the ASR in the rat

Plasticity of spatial hearing: Behavioural effects of cortical inactivation

The contribution of auditory cortex to spatial information processing was explored behaviourally in adult ferrets by reversibly deactivating different cortical areas by subdural placement of a polymer that released the GABA agonist muscimol over a period of weeks. The spatial extent and time course of cortical inactivation were determined electrophysiologically. Muscimol-Elvax was placed bilaterally over the anterior (AEG), middle (MEG) or posterior ectosylvian gyrus (PEG), so that different regions of the auditory cortex could be deactivated in different cases. Sound localization accuracy in the horizontal plane was assessed by measuring both the initial head orienting and approach-to-target responses made by the animals. Head orienting behaviour was unaffected by silencing any region of the auditory cortex, whereas the accuracy of approach-to-target responses to brief sounds (40 ms noise bursts) was reduced by muscimol-Elvax but not by drug-free implants. Modest but significant localization impairments were observed after deactivating the MEG, AEG or PEG, although the largest deficits were produced in animals in which the MEG, where the primary auditory fields are located, was silenced. We also examined experience-induced spatial plasticity by reversibly plugging one ear. In control animals, localization accuracy for both approach-to-target and head orienting responses was initially impaired by monaural occlusion, but recovered with training over the next few days. Deactivating any part of the auditory cortex resulted in less complete recovery than in controls, with the largest deficits observed after silencing the higher-level cortical areas in the AEG and PEG. Although suggesting that each region of auditory cortex contributes to spatial learning, differences in the localization deficits and degree of adaptation between groups imply a regional specialization in the processing of spatial information across the auditory cortex. © 2012 The Authors. The Journal of Physiology © 2012 The Physiological Society

Cortico-cortical connectivity within ferret auditory cortex

Despite numerous studies of auditory cortical processing in the ferret (Mustela putorius), very little is known about the connections between the different regions of the auditory cortex that have been characterized cytoarchitectonically and physiologically. We examined the distribution of retrograde and anterograde labeling after injecting tracers into one or more regions of ferret auditory cortex. Injections of different tracers at frequency-matched locations in the core areas, the primary auditory cortex (A1) and anterior auditory field (AAF), of the same animal revealed the presence of reciprocal connections with overlapping projections to and from discrete regions within the posterior pseudosylvian and suprasylvian fields (PPF and PSF), suggesting that these connections are frequency specific. In contrast, projections from the primary areas to the anterior dorsal field (ADF) on the anterior ectosylvian gyrus were scattered and non-overlapping, consistent with the non-tonotopic organization of this field. The relative strength of the projections originating in each of the primary fields differed, with A1 predominantly targeting the posterior bank fields PPF and PSF, which in turn project to the ventral posterior field, whereas AAF projects more heavily to the ADF, which then projects to the anteroventral field and the pseudosylvian sulcal cortex. These findings suggest that parallel anterior and posterior processing networks may exist, although the connections between different areas often overlap and interactions were present at all levels

Functional organization of ferret auditory cortex.

We characterized the functional organization of different fields within the auditory cortex of anaesthetized ferrets. As previously reported, the primary auditory cortex, A1, and the anterior auditory field, AAF, are located on the middle ectosylvian gyrus. These areas exhibited a similar tonotopic organization, with high frequencies represented at the dorsal tip of the gyrus and low frequencies more ventrally, but differed in that AAF neurons had shorter response latencies than those in A1. On the basis of differences in frequency selectivity, temporal response properties and thresholds, we identified four more, previously undescribed fields. Two of these are located on the posterior ectosylvian gyrus and were tonotopically organized. Neurons in these areas responded robustly to tones, but had longer latencies, more sustained responses and a higher incidence of non-monotonic rate-level functions than those in the primary fields. Two further auditory fields, which were not tonotopically organized, were found on the anterior ectosylvian gyrus. Neurons in the more dorsal anterior area gave short-latency, transient responses to tones and were generally broadly tuned with a preference for high (>8 kHz) frequencies. Neurons in the other anterior area were frequently unresponsive to tones, but often responded vigorously to broadband noise. The presence of both tonotopic and non-tonotopic auditory cortical fields indicates that the organization of ferret auditory cortex is comparable to that seen in other mammals