TRANSFORMATIONS OF TASK-DEPENDENT PLASTICITY FROM A1 TO HIGHER-ORDER AUDITORY CORTEX

Everyday, humans and animals navigate complex acoustic environments, where multiple sound sources overlap. Somehow, they effortlessly perform an acoustic scene analysis and extract relevant signals from background noise. Constant updating of the behavioral relevance of ambient sounds requires the representation and integration of incoming acoustical information with internal representations such as behavioral goals, expectations and memories of previous sound-meaning associations. Rapid plasticity of auditory representations may contribute to our ability to attend and focus on relevant sounds. In order to better understand how auditory representations are transformed in the brain to incorporate behavioral contextual information, we explored task-dependent plasticity in neural responses recorded at four levels of the auditory cortical processing hierarchy of ferrets: the primary auditory cortex (A1), two higher-order auditory areas (dorsal PEG and ventral-anterior PEG) and dorso-lateral frontal cortex. In one study we explored the laminar profile of rapid-task related plasticity in A1 and found that plasticity occurred at all depths, but was greatest in supragranular layers. This result suggests that rapid task-related plasticity in A1 derives primarily from intracortical modulation of neural selectivity. In two other studies we explored task-dependent plasticity in two higher-order areas of the ferret auditory cortex that may correspond to belt (secondary) and parabelt (tertiary) auditory areas. We found that representations of behaviorally-relevant sounds are progressively enhanced during performance of auditory tasks. These selective enhancement effects became progressively larger as you ascend the auditory cortical hierarchy. We also observed neuronal responses to non-auditory, task-related information (reward timing, expectations) in the parabelt area that were very similar to responses previously described in frontal cortex. These results suggests that auditory representations in the brain are transformed from the more veridical spectrotemporal information encoded in earlier auditory stages to a more abstract representation encoding sound behavioral meaning in higher-order auditory areas and dorso-lateral frontal cortex

Computational Neural Modeling of Auditory Cortical Receptive Fields

Previous studies have shown that the auditory cortex can enhance the perception of behaviorally important sounds in the presence of background noise, but the mechanisms by which it does this are not yet elucidated. Rapid plasticity of spectrotemporal receptive fields (STRFs) in the primary (A1) cortical neurons is observed during behavioral tasks that require discrimination of particular sounds. This rapid task-related change is believed to be one of the processing strategies utilized by the auditory cortex to selectively attend to one stream of sound in the presence of mixed sounds. However, the mechanism by which the brain evokes this rapid plasticity in the auditory cortex remains unclear. This paper uses a neural network model to investigate how synaptic transmission within the cortical neuron network can change the receptive fields of individual neurons. A sound signal was used as input to a model of the cochlea and auditory periphery, which activated or inhibited integrate-and-fire neuron models to represent networks in the primary auditory cortex. Each neuron in the network was tuned to a different frequency. All neurons were interconnected with excitatory or inhibitory synapses of varying strengths. Action potentials in one of the model neurons were used to calculate the receptive field using reverse correlation. The results were directly compared to previously recorded electrophysiological data from ferrets performing behavioral tasks that require discrimination of particular sounds. The neural network model could reproduce complex STRFs observed experimentally through optimizing the synaptic weights in the model. The model predicts that altering synaptic drive between cortical neurons and/or bottom-up synaptic drive from the cochlear model to the cortical neurons can account for rapid task-related changes observed experimentally in A1 neurons. By identifying changes in the synaptic drive during behavioral tasks, the model provides insights into the neural mechanisms utilized by the auditory cortex to enhance the perception of behaviorally salient sounds

Auditory Cortex Basal Activity Modulates Cochlear Responses in Chinchillas

Background: The auditory efferent system has unique neuroanatomical pathways that connect the cerebral cortex with sensory receptor cells. Pyramidal neurons located in layers V and VI of the primary auditory cortex constitute descending projections to the thalamus, inferior colliculus, and even directly to the superior olivary complex and to the cochlear nucleus. Efferent pathways are connected to the cochlear receptor by the olivocochlear system, which innervates outer hair cells and auditory nerve fibers. The functional role of the cortico-olivocochlear efferent system remains debated. We hypothesized that auditory cortex basal activity modulates cochlear and auditory-nerve afferent responses through the efferent system. Methodology/Principal Findings: Cochlear microphonics (CM), auditory-nerve compound action potentials (CAP) and auditory cortex evoked potentials (ACEP) were recorded in twenty anesthetized chinchillas, before, during and after auditory cortex deactivation by two methods: lidocaine microinjections or cortical cooling with cryoloops. Auditory cortex deactivation induced a transient reduction in ACEP amplitudes in fifteen animals (deactivation experiments) and a permanent reduction in five chinchillas (lesion experiments). We found significant changes in the amplitude of CM in both types of experiments, being the most common effect a CM decrease found in fifteen animals. Concomitantly to CM amplitude changes, we found CAP increases in seven chinchillas and CAP reductions in thirteen animals. Although ACE

Effects of Electrical Stimulation of Olivocochlear Fibers in Cochlear Potentials in the Chinchilla

The mammalian cochlea has two types of sensory cells; inner hair cells, which receive auditory-nerve afferent innervation, and outer hair cells, innervated by efferent axons of the medial olivocochlear (MOC) system. The role of the MOC system in hearing is still controversial. Recently, by recording cochlear potentials in behaving chinchillas, we suggested that one of the possible functions of the efferent system is to reduce cochlear sensitivity during attention to other sensory modalities (Delano et al. in J Neurosci 27:4146–4153, 2007). However, in spite of these compelling results, the physiological effects of electrical MOC activation on cochlear potentials have not been described in detail in chinchillas. The main objective of the present work was to describe these efferent effects in the chinchilla, comparing them with those in other species and in behavioral experiments. We activated the MOC efferent axons in chinchillas with sectioned middle-ear muscles by applying current pulses at the fourth-ventricle floor. Auditory-nerve compound action potentials (CAP) and cochlear microphonics (CM) were acquired in response to clicks and tones of several frequencies, using a round-window electrode. Electrical efferent stimulation produced CAP amplitude suppressions reaching up to 11 dB. They were higher for low to moderate sound levels. Additionally, CM amplitude increments were found, the largest (≤ 2.5 dB) for low intensity tones. CAP suppression was present at all stimulus frequencies, but was greatest for 2 kHz. CM increments were highest for low-frequency tones, and almost absent at high frequencies. We conclude that the effect obtained in chinchilla is similar to but smaller than that observed in cats, and that the effects seen in awake chinchillas, albeit different in magnitude, are consistent with the activation of efferent fibers

Laminar profile of task-related plasticity in ferret primary auditory cortex

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Schematic representation of the working model for corticofugal modulation of cochlear and auditory nerve responses produced by auditory cortex deactivation.

<p>The magnitude of cortical deactivation (green shade) produced by cryoloops (B) was larger than the one produced by lidocaine microinjections (A). Based on previous studies <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036203#pone.0036203-Feliciano1" target="_blank">[48]</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036203#pone.0036203-Bajo1" target="_blank">[50]</a> we propose the presence of an excitatory basal tone mediated by two groups of glutamatergic pyramidal neurons. In this model, pyramidal neurons located in auditory cortex layers V and VI project through parallel pathways to the inferior colliculus (IC). These cortical neurons are differentially deactivated (represented in light-blue) by lidocaine or cryoloops. There is indirect evidence of excitatory connections from the IC to MOC neurons <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036203#pone.0036203-Mulders3" target="_blank">[52]</a>, but it is unknown whether there is another parallel pathway from IC to the LOC (? mark in the model). In this working model, a complete loss of descending excitatory activity will lead to CAP and CM reduction, as was observed in most cryoloop experiments. On the other hand, random deactivation of different subsets of pyramidal neurons could lead to CAP and CM enhancements or reductions, depending on the population of neurons deactivated. Blue arrows from CM to CAP represent an alternative hypothesis to explain CAP changes. Corticofugal modulation of outer hair cell activity can alter cochlear functioning and thus auditory nerve responses. (I–VI: auditory cortex layers; wm: white matter; glu: glutamate; IC: inferior colliculus).</p

Temporal course of CAP, CM and ACEP changes before, during and after auditory cortex cooling at 3°C with cryoloops.

<p>Amplitude changes in CM (blue squares), CAP (red circles) and ACEP (black triangles) are depicted in dB referenced to the mean baseline amplitude prior cortical cooling. In this experiment, 2 kHz stimuli were presented at different sound pressure levels, represented by symbols sizes increasing in 10 dB steps from 40 to 90 dB SPL. Cyan shaded areas illustrate the period of cortical cryoloop cooling at 3°C. <b>A. Amplitude changes in cochlear potentials.</b> Auditory cortex cooling produced significant CAP and CM amplitude reductions (F = 50.42, p<0.001 and F = 132.66, p<0.001 respectively), which were largest for low and moderate sound pressure levels. Tukey post-hoc tests revealed significant CAP and CM amplitude differences between the three periods studied (baseline, cooling and recovery). <b>B. Auditory-cortex evoked potentials amplitude changes.</b> Cortical cooling reduced ACEP amplitudes down to −25 dB. Note that 40 to 60 minutes after the end of cortical cooling there was a complete recovery of evoked potentials, but there was no recovery in cochlear potentials amplitudes.</p

Summary of results.

<p>The largest changes in CAP, CM and ACEP measured in dB for each experiment. Deactivation experiments included fifteen animals (n = 1–15) but seventeen ears, as there were two bilateral experiments. Five chinchillas were tested in lesion experiments (n = 16–20). Exp_ID: Identification of experiments. L: lidocaine experiments. C°: cortical temperature of cryoloop experiments.</p

Temporal course and sound pressure dependency of amplitude changes in cochlear and cortical potentials after lidocaine cortical deactivation.

<p>Amplitude changes are depicted in dB referenced to baseline amplitude before lidocaine microinjection for CM (blue squares), CAP (red circles) and ACEP (black triangles). In this experiment, 6 kHz stimuli were presented at different sound pressure levels. Different symbol sizes represent stimulus sound pressure level, increasing in 10 dB steps from 30 to 90 dB SPL. Significant CAP and CM increases (t = −3.22, p<0.01 and t = −10.13, p<0.001 respectively) were obtained, after a 3 µl lidocaine microinjection (green arrow) in the contralateral auditory cortex. The largest effects on CM and CAP were found with low intensity sounds. Note that CM and CAP increases are maintained after the recovery of cortical evoked potentials. Note also that sixty minutes after the lidocaine microinjection, an inverted effect was observed for CAP obtained at high intensity levels (80–90 dB SPL). (Exp_ID: cx_rw_14).</p

Summary of contralateral corticofugal effects obtained with lidocaine and cryoloop deactivation experiments.

<p>A scatter plot of maximum CAP and CM amplitude changes obtained with both deactivation methods is shown (green circles: lidocaine; blue squares: cryoloops). The most common effect was a simultaneous reduction in CM and CAP, observed in ten experiments. Parallel effects (correlative increases or decreases) were obtained in twelve animals, while dissociated effects were seen in three. Note that lidocaine deactivation produced diverse types of CAP and CM amplitude changes (reductions and increases), while most of the cryoloop experiments produced significant CM and CAP reductions.</p