Plasticity and corticofugal modulation for hearing in adult animals

The descending (corticofugal) auditory system adjusts and improves auditory signal processing in the subcortical auditory nuclei. The auditory cortex and corticofugal system evoke small, short-term changes of the subcortical auditory nuclei in response to a sound repetitively delivered to an animal. These changes are specific to the parameters characterizing the sound. When the sound becomes significant to the animal through conditioning (associative learning), the changes are augmented and the cortical changes become long-term. There are two types of reorganizations: expanded reorganization resulting from centripetal shifts in tuning curves of neurons toward the values of the parameters characterizing a sound and compressed reorganization resulting from centrifugal shifts in tuning curves of neurons away from these values. The two types of reorganizations are based on a single mechanism consisting of two components: facilitation and inhibition.     

Corticofugal regulation of auditory sensitivity in the bat inferior colliculus

Under free-field stimulation conditions, corticofugal regulation of auditory sensitivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus, was studied by blocking activities of auditory cortical neurons with Lidocaine or by electrical stimulation in auditory cortical neuron recording sites. The corticocollicular pathway regulated the number of impulses, the auditory spatial response areas and the frequency-tuning curves of inferior colliculus neurons through facilitation or inhibition. Corticofugal regulation was most effective at low sound intensity and was dependent upon the time interval between acoustic and electrical stimuli. At optimal interstimulus intervals, inferior colliculus neurons had the smallest number of impulses and the longest response latency during corticofugal inhibition. The opposite effects were observed during corticofugal facilitation. Corticofugal inhibitory latency was longer than corticofugal facilitatory latency. Iontophoretic application of γ-aminobutyric acid and bicuculline to inferior colliculus recording sites produced effects similar to what were observed during corticofugal inhibition and facilitation. We suggest that corticofugal regulation of central auditory sensitivity can provide an animal with a mechanism to regulate acoustic signal processing in the ascending auditory pathway. Accepted: 15 July 1998     

Corticofugal modulation of initial neural processing of sound information from the ipsilateral ear in the mouse

Background

Cortical neurons implement a high frequency-specific modulation of subcortical nuclei that includes the cochlear nucleus. Anatomical studies show that corticofugal fibers terminating in the auditory thalamus and midbrain are mostly ipsilateral. Differently, corticofugal fibers terminating in the cochlear nucleus are bilateral, which fits to the needs of binaural hearing that improves hearing quality. This leads to our hypothesis that corticofugal modulation of initial neural processing of sound information from the contralateral and ipsilateral ears could be equivalent or coordinated at the first sound processing level.

Methodology/Principal Findings

With the focal electrical stimulation of the auditory cortex and single unit recording, this study examined corticofugal modulation of the ipsilateral cochlear nucleus. The same methods and procedures as described in our previous study of corticofugal modulation of contralateral cochlear nucleus were employed simply for comparison. We found that focal electrical stimulation of cortical neurons induced substantial changes in the response magnitude, response latency and receptive field of ipsilateral cochlear nucleus neurons. Cortical stimulation facilitated auditory response and shortened the response latency of physiologically matched neurons whereas it inhibited auditory response and lengthened the response latency of unmatched neurons. Finally, cortical stimulation shifted the best frequencies of cochlear neurons towards those of stimulated cortical neurons.

Conclusion

Our data suggest that cortical neurons enable a high frequency-specific remodelling of sound information processing in the ipsilateral cochlear nucleus in the same manner as that in the contralateral cochlear nucleus.     

Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.     

Noninvasive fMRI Investigation of Interaural Level Difference Processing in the Rat Auditory Subcortex

Objective

Interaural level difference (ILD) is the difference in sound pressure level (SPL) between the two ears and is one of the key physical cues used by the auditory system in sound localization. Our current understanding of ILD encoding has come primarily from invasive studies of individual structures, which have implicated subcortical structures such as the cochlear nucleus (CN), superior olivary complex (SOC), lateral lemniscus (LL), and inferior colliculus (IC). Noninvasive brain imaging enables studying ILD processing in multiple structures simultaneously.

Methods

In this study, blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) is used for the first time to measure changes in the hemodynamic responses in the adult Sprague-Dawley rat subcortex during binaural stimulation with different ILDs.

Results and Significance

Consistent responses are observed in the CN, SOC, LL, and IC in both hemispheres. Voxel-by-voxel analysis of the change of the response amplitude with ILD indicates statistically significant ILD dependence in dorsal LL, IC, and a region containing parts of the SOC and LL. For all three regions, the larger amplitude response is located in the hemisphere contralateral from the higher SPL stimulus. These findings are supported by region of interest analysis. fMRI shows that ILD dependence occurs in both hemispheres and multiple subcortical levels of the auditory system. This study is the first step towards future studies examining subcortical binaural processing and sound localization in animal models of hearing.     

Changes in early cortical visual processing predict enhanced reactivity in deaf individuals

Individuals with profound deafness rely critically on vision to interact with their environment. Improvement of visual performance as a consequence of auditory deprivation is assumed to result from cross-modal changes occurring in late stages of visual processing. Here we measured reaction times and event-related potentials (ERPs) in profoundly deaf adults and hearing controls during a speeded visual detection task, to assess to what extent the enhanced reactivity of deaf individuals could reflect plastic changes in the early cortical processing of the stimulus. We found that deaf subjects were faster than hearing controls at detecting the visual targets, regardless of their location in the visual field (peripheral or peri-foveal). This behavioural facilitation was associated with ERP changes starting from the first detectable response in the striate cortex (C1 component) at about 80 ms after stimulus onset, and in the P1 complex (100-150 ms). In addition, we found that P1 peak amplitudes predicted the response times in deaf subjects, whereas in hearing individuals visual reactivity and ERP amplitudes correlated only at later stages of processing. These findings show that long-term auditory deprivation can profoundly alter visual processing from the earliest cortical stages. Furthermore, our results provide the first evidence of a co-variation between modified brain activity (cortical plasticity) and behavioural enhancement in this sensory-deprived population.     

Perceptual organization of sound begins in the auditory periphery

Segmenting the complex acoustic mixture that makes a typical auditory scene into relevant perceptual objects is one of the main challenges of the auditory system [1], for both human and nonhuman species. Several recent studies indicate that perceptual auditory object formation, or "streaming," may be based on neural activity within the auditory cortex and beyond [2, 3]. Here, we find that scene analysis starts much earlier in the auditory pathways. Single units were recorded from a peripheral structure of the mammalian auditory brainstem, the cochlear nucleus. Peripheral responses were similar to cortical responses and displayed all of the functional properties required for streaming, including multisecond adaptation. Behavioral streaming was also measured in human listeners. Neurometric functions derived from the peripheral responses predicted accurately behavioral streaming. This reveals that subcortical structures may already contribute to the analysis of auditory scenes. This finding is consistent with the observation that species lacking a neocortex can still achieve and benefit from behavioral streaming [4]. For humans, we argue that auditory scene analysis of complex scenes is probably based on interactions between subcortical and cortical neural processes, with the relative contribution of each stage depending on the nature of the acoustic cues forming the streams.     

Learning-induced plasticity in animal and human auditory cortex

Recent data on learning-related changes in animal and human auditory cortex indicate functions beyond mere stimulus representation and simple recognition memory for stimuli. Rather, auditory cortex seems to process and represent stimuli in a task-dependent fashion. This implies plasticity in neural processing, which can be observed at the level of single neuron firing and the level of spatiotemporal activity patterns in cortical areas. Auditory cortex is a structure in which behaviorally relevant aspects of stimulus processing are highly developed because of the fugitive nature of auditory stimuli.     

Hearing it again and again: on-line subcortical plasticity in humans

Background

Human brainstem activity is sensitive to local sound statistics, as reflected in an enhanced response in repetitive compared to pseudo-random stimulus conditions [1]. Here we probed the short-term time course of this enhancement using a paradigm that assessed how the local sound statistics (i.e., repetition within a five-note melody) interact with more global statistics (i.e., repetition of the melody).

Methodology/Principal Findings

To test the hypothesis that subcortical repetition enhancement builds over time, we recorded auditory brainstem responses in young adults to a five-note melody containing a repeated note, and monitored how the response changed over the course of 1.5 hrs. By comparing response amplitudes over time, we found a robust time-dependent enhancement to the locally repeating note that was superimposed on a weaker enhancement of the globally repeating pattern.

Conclusions/Significance

We provide the first demonstration of on-line subcortical plasticity in humans. This complements previous findings that experience-dependent subcortical plasticity can occur on a number of time scales, including life-long experiences with music and language, and short-term auditory training. Our results suggest that the incoming stimulus stream is constantly being monitored, even when the stimulus is physically invariant and attention is directed elsewhere, to augment the neural response to the most statistically salient features of the ongoing stimulus stream. These real-time transformations, which may subserve humans'' strong disposition for grouping auditory objects, likely reflect a mix of local processes and corticofugal modulation arising from statistical regularities and the influences of expectation. Our results contribute to our understanding of the biological basis of statistical learning and initiate a new investigational approach relating to the time-course of subcortical plasticity. Although the reported time-dependent enhancements are believed to reflect universal neurophysiological processes, future experiments utilizing a larger array of stimuli are needed to establish the generalizability of our findings.     

Direction-dependent corticofugal modulation of frequency-tuning curves of inferior collicular neurons in the big brown bat, Eptesicus fuscus

This study examined if corticofugal modulation of subcortical frequency-tuning curves varied with sound direction. Both excitatory and inhibitory frequency tuning curves of inferior collicular neurons of the big brown bat, Eptesicus fuscus were plotted before and during electrical stimulation in the auditory cortex at two sound directions (contra-40 degrees and ipsi-40 degrees). Most collicular neurons had broader excitatory frequency-tuning curves at contra-40 degrees but had broader inhibitory frequency-tuning curves at ipsi-40 degrees. Cortical electrical stimulation changed the excitatory minimum thresholds of most collicular neurons at a greater degree at ipsi-40 degrees than at contra-40 degrees. However, cortical electrical stimulation produced a greater increase in the sharpness of excitatory frequency-tuning curves of most corticofugally inhibited collicular neurons at contra-40 degrees but produced a greater decrease in the sharpness of excitatory frequency-tuning curves of most corticofugally facilitated collicular neurons at ipsi-40 degrees. Cortical electrical stimulation also produced a greater change in the sharpness of inhibitory frequency-tuning curves of most corticofugally inhibited collicular neurons at contra-40 degrees than at ipsi-40 degrees. Possible mechanisms for this direction-dependent corticofugal modulation of frequency-tuning curves of collicular neurons are discussed.     

Temporal Sequence of Visuo-Auditory Interaction in Multiple Areas of the Guinea Pig Visual Cortex

Recent studies in humans and monkeys have reported that acoustic stimulation influences visual responses in the primary visual cortex (V1). Such influences can be generated in V1, either by direct auditory projections or by feedback projections from extrastriate cortices. To test these hypotheses, cortical activities were recorded using optical imaging at a high spatiotemporal resolution from multiple areas of the guinea pig visual cortex, to visual and/or acoustic stimulations. Visuo-auditory interactions were evaluated according to differences between responses evoked by combined auditory and visual stimulation, and the sum of responses evoked by separate visual and auditory stimulations. Simultaneous presentation of visual and acoustic stimulations resulted in significant interactions in V1, which occurred earlier than in other visual areas. When acoustic stimulation preceded visual stimulation, significant visuo-auditory interactions were detected only in V1. These results suggest that V1 is a cortical origin of visuo-auditory interaction.     

Cortical motion deafness

The extent to which the auditory system, like the visual system, processes spatial stimulus characteristics such as location and motion in separate specialized neuronal modules or in one homogeneously distributed network is unresolved. Here we present a patient with a selective deficit for the perception and discrimination of auditory motion following resection of the right anterior temporal lobe and the right posterior superior temporal gyrus (STG). Analysis of stimulus identity and location within the auditory scene remained intact. In addition, intracranial auditory evoked potentials, recorded preoperatively, revealed motion-specific responses selectively over the resected right posterior STG, and electrical cortical stimulation of this region was experienced by the patient as incoming moving sounds. Collectively, these data present a patient with cortical motion deafness, providing evidence that cortical processing of auditory motion is performed in a specialized module within the posterior STG.     

Cortical processing and perceived timing

As of yet, it is unclear how we determine relative perceived timing. One controversial suggestion is that timing perception might be related to when analyses are completed in the cortex of the brain. An alternate proposal suggests that perceived timing is instead related to the point in time at which cortical analyses commence. Accordingly, timing illusions should not occur owing to cortical analyses, but they could occur if there were differential delays between signals reaching cortex. Resolution of this controversy therefore requires that the contributions of cortical processing be isolated from the influence of subcortical activity. Here, we have done this by using binocular disparity changes, which are known to be detected via analyses that originate in cortex. We find that observers require longer stimulus exposures to detect small, relative to larger, disparity changes; observers are slower to react to smaller disparity changes and observers misperceive smaller disparity changes as being perceptually delayed. Interestingly, disparity magnitude influenced perceived timing more dramatically than it did stimulus change detection. Our data therefore suggest that perceived timing is both influenced by cortical processing and is shaped by sensory analyses subsequent to those that are minimally necessary for stimulus change perception.     

Cortico-subcortical interrelationships in the visual analyzer system at various stages of ontogenesis]

The influence of a corticofugal volley produced by single electrical stimulation of the visual projection cortical zone on the neuronal activity of LGB was studied in non-anaesthetized rabbits aged from three to thirty-five days. A coincidence was found between the time of appearance of nonspecific inhibitory corticofugal influences on the spontaneous activity of LGB neurons and the emergence of the first phasic-specific responses of the neurones of this level to a visual stimulus. It has been shown that the sensory flow at the LGB level can be controlled by non-specific inhibitory corticofugal influences at early periods of postnatal development. The appearance from the 15th day of life of specific responses to a corticofugal volley, including activation phases, leads to a greater complexity of the regulating Cortical influences on conduction of the afferent signal at the thalamic level. The data obtained are considered from the standpoint of integration of various levels of the visual analyser at different stages of ontogenesis.     

Response variability in the mammalian auditory cortex: an objection to feature detection?

Research strategy in the auditory system has tended to parallel that in the visual system, where neurons have been shown to respond selectively to specific stimulus parameters. Auditory neurons have been shown to be sensitive to changes in acoustic parameters, but only rarely have neurons been reported that respond exclusively to only one biologically significant sound. Even at higher levels of the auditory system very few cells have been found that could be described as "vocalization detectors." In addition, variability in responses to artificial sounds have been reported for auditory cortical neurons similar to the response variability that has been reported in the visual system. Recent evidence indicates that the responses of auditory cortical neurons to species-specific vocalizations can also be labile, varying in both strength and selectivity. This is especially true of the secondary auditory cortex. This variability, coupled with the lack of extreme specificity in the secondary auditory cortex, suggests that secondary cortical neurons are not well suited for the role of "vocalization detectors."     

Selective Attention Modulates Human Auditory Brainstem Responses: Relative Contributions of Frequency and Spatial Cues

Selective attention is the mechanism that allows focusing one’s attention on a particular stimulus while filtering out a range of other stimuli, for instance, on a single conversation in a noisy room. Attending to one sound source rather than another changes activity in the human auditory cortex, but it is unclear whether attention to different acoustic features, such as voice pitch and speaker location, modulates subcortical activity. Studies using a dichotic listening paradigm indicated that auditory brainstem processing may be modulated by the direction of attention. We investigated whether endogenous selective attention to one of two speech signals affects amplitude and phase locking in auditory brainstem responses when the signals were either discriminable by frequency content alone, or by frequency content and spatial location. Frequency-following responses to the speech sounds were significantly modulated in both conditions. The modulation was specific to the task-relevant frequency band. The effect was stronger when both frequency and spatial information were available. Patterns of response were variable between participants, and were correlated with psychophysical discriminability of the stimuli, suggesting that the modulation was biologically relevant. Our results demonstrate that auditory brainstem responses are susceptible to efferent modulation related to behavioral goals. Furthermore they suggest that mechanisms of selective attention actively shape activity at early subcortical processing stages according to task relevance and based on frequency and spatial cues.     

听觉皮层信号处理

听觉系统和视觉系统的不同之处在于：听觉系统在外周感受器和听皮层间具有更长的皮层下通路和更多的突触联系。该特殊结构反应了听觉系统从复杂听觉环境中提取与行为相关信号的机制与其他感觉系统不同。听皮层神经信号处理包括两种重要的转换机制,声音信号的非同构转换以及从声音感受到知觉层面的转换。听觉皮层神经编码机制同时也受到听觉反馈和语言或发声过程中发声信号的调控。听觉神经科学家和生物医学工程师所面临的挑战便是如何去理解大脑中这些转换的编码机制。我将会用我实验室最近的一些发现来阐述听觉信号是如何在原听皮层中进行处理的,并讨论其对于言语和音乐在大脑中的处理机制以及设计神经替代装置诸如电子耳蜗的意义。我们使用了结合神经电生理技术和量化工程学的方法来研究这些问题。     

Neural modulation in inferior colliculus and central auditory plasticity

The neural modulation in central auditory system plays an important role in perception and processing of sound signal and auditory cognition. The inferior colliculus (IC) is both a relay station in central auditory pathway and a sub-cortical auditory center doing the sound signal processing. IC is also modulated by the descending projections from the cortex and auditory thalamus, medial geniculate body, and these neural modulations not only can affect ongoing sound signal processing but can also induce plastic changes in IC.     

Conditional tonic stimulus control of nonspecific arousal

Subjects performed a reaction time (RT) task in the presence of colored indirect lighting which had previously been associated with either sporadic electric shock (Unsafe context) or no shock (Safe context). Autonomic and cortical processes were influenced by the visual context in two ways. Nonspecific arousal was elevated in the Unsafe context as compared with the Safe context (larger SCR and more accelerative HR change elicited by the RT warning stimulus, and retarded habituation of the middle component of the slow cortical potential during the warning stimulus). In addition, information processing may have been impaired in the Unsafe as compared to the Safe context, since the earliest component of the SCR and the N100 component of the auditory evoked potential were both reduced. Higher frequency of unelicited SCR was observed following changes from a Safe to an Unsafe context than with reverse changes, during the association of these contexts with shock, but this was the only evidence of direct tonic conditioning. In general, the results demonstrate the degree to which psychophysiological processes may be influenced by tonic environmental conditions.     

Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands

Studies analyzing sensory cortical processing or trying to decode brain activity often rely on a combination of different electrophysiological signals, such as local field potentials (LFPs) and spiking activity. Understanding the relation between these signals and sensory stimuli and between different components of these signals is hence of great interest. We here provide an analysis of LFPs and spiking activity recorded from visual and auditory cortex during stimulation with natural stimuli. In particular, we focus on the time scales on which different components of these signals are informative about the stimulus, and on the dependencies between different components of these signals. Addressing the first question, we find that stimulus information in low frequency bands (<12 Hz) is high, regardless of whether their energy is computed at the scale of milliseconds or seconds. Stimulus information in higher bands (>50 Hz), in contrast, is scale dependent, and is larger when the energy is averaged over several hundreds of milliseconds. Indeed, combined analysis of signal reliability and information revealed that the energy of slow LFP fluctuations is well related to the stimulus even when considering individual or few cycles, while the energy of fast LFP oscillations carries information only when averaged over many cycles. Addressing the second question, we find that stimulus information in different LFP bands, and in different LFP bands and spiking activity, is largely independent regardless of time scale or sensory system. Taken together, these findings suggest that different LFP bands represent dynamic natural stimuli on distinct time scales and together provide a potentially rich source of information for sensory processing or decoding brain activity.