Activity In Auditory Cortex Research Articles

Neural correlates of visual stimulus encoding and verbal working memory differ between cochlear implant users and normal-hearing controls.

A common concern for individuals with severe‐to‐profound hearing loss fitted with cochlear implants (CIs) is difficulty following conversations in noisy environments. Recent work has suggested that these difficulties are related to individual differences in brain function, including verbal working memory and the degree of cross‐modal reorganization of auditory areas for visual processing. However, the neural basis for these relationships is not fully understood. Here, we investigated neural correlates of visual verbal working memory and sensory plasticity in 14 CI users and age‐matched normal‐hearing (NH) controls. While we recorded the high‐density electroencephalogram (EEG), participants completed a modified Sternberg visual working memory task where sets of letters and numbers were presented visually and then recalled at a later time. Results suggested that CI users had comparable behavioural working memory performance compared with NH. However, CI users had more pronounced neural activity during visual stimulus encoding, including stronger visual‐evoked activity in auditory and visual cortices, larger modulations of neural oscillations and increased frontotemporal connectivity. In contrast, during memory retention of the characters, CI users had descriptively weaker neural oscillations and significantly lower frontotemporal connectivity. We interpret the differences in neural correlates of visual stimulus processing in CI users through the lens of cross‐modal and intramodal plasticity.

Neurophysiological Evaluation of Right-Ear Advantage During Dichotic Listening.

Right-ear advantage refers to the observation that when two different speech stimuli are simultaneously presented to both ears, listeners report stimuli more correctly from the right ear than the left. It is assumed to result from prominent projection along the auditory pathways to the contralateral hemisphere and the dominance of the left auditory cortex for the perception of speech elements. Our study aimed to investigate the role of attention in the right-ear advantage. We recorded magnetoencephalography data while participants listened to pairs of Japanese two-syllable words (namely, “/ta/ /ko/” or “/i/ /ka/”). The amplitudes of the stimuli were modulated at 35 Hz in one ear and 45 Hz in the other. Such frequency-tagging allowed the selective quantification of left and right auditory cortex responses to left and right ear stimuli. Behavioral tests confirmed the right-ear advantage, with higher accuracy for stimuli presented to the right ear than to the left. The amplitude of the auditory steady-state response was larger when attending to the stimuli compared to passive listening. We detected a correlation between the attention-related increase in the amplitude of the auditory steady-state response and the laterality index of behavioral accuracy. The right-ear advantage in the free-response dichotic listening was also found in neural activities in the left auditory cortex, suggesting that it was related to the allocation of attention to both ears.

Action-locked Neural Responses in Auditory Cortex to Self-generated Sounds.

Sensory perception is a product of interactions between the internal state of an organism and the physical attributes of a stimulus. It has been shown across the animal kingdom that perception and sensory-evoked physiological responses are modulated depending on whether or not the stimulus is the consequence of voluntary actions. These phenomena are often attributed to motor signals sent to relevant sensory regions that convey information about upcoming sensory consequences. However, the neurophysiological signature of action-locked modulations in sensory cortex, and their relationship with perception, is still unclear. In the current study, we recorded neurophysiological (using Magnetoencephalography) and behavioral responses from 16 healthy subjects performing an auditory detection task of faint tones. Tones were either generated by subjects' voluntary button presses or occurred predictably following a visual cue. By introducing a constant temporal delay between button press/cue and tone delivery, and applying source-level analysis, we decoupled action-locked and auditory-locked activity in auditory cortex. We show action-locked evoked-responses in auditory cortex following sound-triggering actions and preceding sound onset. Such evoked-responses were not found for button-presses that were not coupled with sounds, or sounds delivered following a predictive visual cue. Our results provide evidence for efferent signals in human auditory cortex that are locked to voluntary actions coupled with future auditory consequences.

Subcortical circuits mediate communication between primary sensory cortical areas in mice

Integration of information across the senses is critical for perception and is a common property of neurons in the cerebral cortex, where it is thought to arise primarily from corticocortical connections. Much less is known about the role of subcortical circuits in shaping the multisensory properties of cortical neurons. We show that stimulation of the whiskers causes widespread suppression of sound-evoked activity in mouse primary auditory cortex (A1). This suppression depends on the primary somatosensory cortex (S1), and is implemented through a descending circuit that links S1, via the auditory midbrain, with thalamic neurons that project to A1. Furthermore, a direct pathway from S1 has a facilitatory effect on auditory responses in higher-order thalamic nuclei that project to other brain areas. Crossmodal corticofugal projections to the auditory midbrain and thalamus therefore play a pivotal role in integrating multisensory signals and in enabling communication between different sensory cortical areas.

Cortical Responses to Vowel Sequences in Awake and Anesthetized States: A Human Intracranial Electrophysiology Study.

Elucidating neural signatures of sensory processing across consciousness states is a major focus in neuroscience. Noninvasive human studies using the general anesthetic propofol reveal differential effects on auditory cortical activity, with a greater impact on nonprimary and auditory-related areas than primary auditory cortex. This study used intracranial electroencephalography to examine cortical responses to vowel sequences during induction of general anesthesia with propofol. Subjects were adult neurosurgical patients with intracranial electrodes placed to identify epileptic foci. Data were collected before electrode removal surgery. Stimuli were vowel sequences presented in a target detection task during awake, sedated, and unresponsive states. Averaged evoked potentials (AEPs) and high gamma (70-150Hz) power were measured in auditory, auditory-related, and prefrontal cortex. In the awake state, AEPs were found throughout studied brain areas; high gamma activity was limited to canonical auditory cortex. Sedation led to a decrease in AEP magnitude. Upon LOC, there was a decrease in the superior temporal gyrus and adjacent auditory-related cortex and a further decrease in AEP magnitude in core auditory cortex, changes in the temporal structure and increased trial-to-trial variability of responses. The findings identify putative biomarkers of LOC and serve as a foundation for future investigations of altered sensory processing.

Short-Term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

Chronic vagus nerve stimulation (VNS) has been shown to facilitate learning, but effects of acute VNS on neural coding and behavior remain less well understood. Ferrets implanted with cuff electrodes on the vagus nerve were trained by classical conditioning on an auditory tone frequency-reward association. One tone was associated with reward while another tone was not. Tone frequencies and reward associations were changed every 2 d, requiring learning of a new relationship. When tones were paired with VNS, animals consistently learned the new association within 2 d. When VNS occurred randomly between trials, learning within 2 d was unreliable. In passively listening animals, neural activity in primary auditory cortex (A1) and pupil size were recorded before and after acute VNS-tone pairing. After pairing with a neuron’s best-frequency (BF) tone, responses by a subpopulation of neurons were reduced. VNS paired with an off-BF tone or during intertrial intervals had no effect. The BF-specific reduction in neural responses after VNS remained, even after regressing out changes explained by pupil-indexed arousal. VNS induced brief dilation in the pupil, and the size of this change predicted the magnitude of persistent changes in the neural response. This interaction suggests that fluctuations in neuromodulation associated with arousal gate the long-term VNS effects on neural activity.

Simultaneous Mapping of Neural Activities in Auditory and Visual Cortex of Rat

Simultaneous Mapping of Neural Activities in Auditory and Visual Cortex of Rat

The causal role of auditory cortex in auditory working memory.

Working memory (WM), the ability to actively hold information in memory over a delay period of seconds, is a fundamental constituent of cognition. Delay-period activity in sensory cortices has been observed in WM tasks, but whether and when the activity plays a functional role for memory maintenance remains unclear. Here, we investigated the causal role of auditory cortex (AC) for memory maintenance in mice performing an auditory WM task. Electrophysiological recordings revealed that AC neurons were active not only during the presentation of the auditory stimulus but also early in the delay period. Furthermore, optogenetic suppression of neural activity in AC during the stimulus epoch and early delay period impaired WM performance, whereas suppression later in the delay period did not. Thus, AC is essential for information encoding and maintenance in auditory WM task, especially during the early delay period.

Participation of the Anterior Cingulate Cortex in Sodium Salicylate-induced Tinnitus.

The anterior cingulate cortex (ACC) participates in sodium salicylate (SS)-induced tinnitus through alteration of the disordered neural activity and modulates the neuronal changes in the auditory cortex (AC). Although the mechanism underlying tinnitus remains unclear, the crucial roles of the auditory center and limbic system in this process have been elucidated. Recent reports suggest that dysfunction of the ACC, an important component of the limbic system that regulates and controls the conduction of multiple sensations, is involved in tinnitus. Although altered functional connectivity between the ACC and the auditory system has been observed in humans with tinnitus, the underlying neuronal mechanism remains unexplored. SS (350 mg/kg, 10%, i.p.) was used to yield tinnitus model in rats, followed by comparison of the alteration in the spontaneous firing rate (SFR), local field potential (LFP), and extracellular glutamic acid in the ACC. The responses of neurons in the AC to electrical stimulation from the ACC were also observed. We determined significant increases in the neuronal SFR and extracellular glutamate level in the ACC after SS injection (p < 0.05). These effects were accompanied by decreased alpha band activity and increased beta and gamma band activity (p < 0.05). In the majority of AC neurons, the SFR decreased in response to ACC stimulation (p < 0.05). Our results demonstrated that disordered neural activity in the ACC contributes to SS-induced tinnitus and that ACC activation can modulate AC activity.

Effects of Locomotion in Auditory Cortex Are Not Mediated by the VIP Network.

Movement has a prominent impact on activity in sensory cortex, but has opposing effects on visual and auditory cortex. Both cortical areas feature a vasoactive intestinal peptide-expressing (VIP) disinhibitory circuit, which in visual cortex contributes to the effect of running. In auditory cortex, however, the role of VIP circuitry in running effects remains poorly understood. Running and optogenetic VIP activation are known to differentially modulate sound-evoked activity in auditory cortex, but it is unknown how these effects vary across cortical layers, and whether laminar differences in the roles of VIP circuitry could contribute to the substantial diversity that has been observed in the effects of both movement and VIP activation. Here we asked whether VIP neurons contribute to the effects of running, across the layers of auditory cortex. We found that both running and optogenetic activation of VIP neurons produced diverse changes in the firing rates of auditory cortical neurons, but with distinct effects on spontaneous and evoked activity and with different patterns across cortical layers. On average, running increased spontaneous firing rates but decreased evoked firing rates, resulting in a reduction of the neuronal encoding of sound. This reduction in sound encoding was observed in all cortical layers, but was most pronounced in layer 2/3. In contrast, VIP activation increased both spontaneous and evoked firing rates, and had no net population-wide effect on sound encoding, but strongly suppressed sound encoding in layer 4 narrow-spiking neurons. These results suggest that VIP activation and running act independently, which we then tested by comparing the arithmetic sum of the two effects measured separately to the actual combined effect of running and VIP activation, which were closely matched. We conclude that the effects of locomotion in auditory cortex are not mediated by the VIP network.

Language Proficiency Entails Tuning Cortical Activity to Second Language Speech.

Cortical tracking of linguistic structures in speech, such as phrases (<3Hz, delta band) and syllables (3-8Hz, theta band), is known to be crucial for speech comprehension. However, it has not been established whether this effect is related to language proficiency. Here, we investigate how auditory cortical activity in second language (L2) learners tracked L2 speech. Using magnetoencephalography, we recorded brain activity from participants listening to Spanish and Basque. Participants were Spanish native (L1) language speakers studying Basque (L2) at the same language center at three different levels: beginner (Grade 1), intermediate (Grade 2), and advanced (Grade 3). We found that 1) both delta and theta tracking to L2 speech in the auditory cortex were related to L2 learning proficiency and that 2) top-down modulations of activity in the left auditory regions during L2 speech listening-by the left inferior frontal and motor regions in delta band and by the left middle temporal regions in theta band-were also related to L2 proficiency. Altogether, these results indicate that the ability to learn an L2 is related to successful cortical tracking of L2 speech and its modulation by neuronal oscillations in higher-order cortical regions.

Choice-related activity and neural encoding in primary auditory cortex and lateral belt during feature-selective attention.

Selective attention is necessary to sift through, form a coherent percept of, and make behavioral decisions on the vast amount of information present in most sensory environments. How and where selective attention is employed in cortex and how this perceptual information then informs the relevant behavioral decisions is still not well understood. Studies probing selective attention and decision-making in visual cortex have been enlightening as to how sensory attention might work in that modality; whether or not similar mechanisms are employed in auditory attention is not yet clear. Therefore, we trained rhesus macaques on a feature-selective attention task, where they switched between reporting changes in temporal (amplitude modulation, AM) and spectral (carrier bandwidth) features of a broadband noise stimulus. We investigated how the encoding of these features by single neurons in primary (A1) and secondary (middle lateral belt, ML) auditory cortex was affected by the different attention conditions. We found that neurons in A1 and ML showed mixed selectivity to the sound and task features. We found no difference in AM encoding between the attention conditions. We found that choice-related activity in both A1 and ML neurons shifts between attentional conditions. This finding suggests that choice-related activity in auditory cortex does not simply reflect motor preparation or action and supports the relationship between reported choice-related activity and the decision and perceptual process.NEW & NOTEWORTHY We recorded from primary and secondary auditory cortex while monkeys performed a nonspatial feature attention task. Both areas exhibited rate-based choice-related activity. The manifestation of choice-related activity was attention dependent, suggesting that choice-related activity in auditory cortex does not simply reflect arousal or motor influences but relates to the specific perceptual choice.

Interhemispheric Auditory Cortical Synchronization in Asymmetric Hearing Loss.

Objectives:Auditory cortical activation of the two hemispheres to monaurally presented tonal stimuli has been shown to be asynchronous in normal hearing (NH) but synchronous in the extreme case of adult-onset asymmetric hearing loss (AHL) with single-sided deafness. We addressed the wide knowledge gap between these two anchoring states of interhemispheric temporal organization. The objectives of this study were as follows: (1) to map the trajectory of interhemispheric temporal reorganization from asynchrony to synchrony using magnitude of interaural threshold difference as the independent variable in a cross-sectional study and (2) to evaluate reversibility of interhemispheric synchrony in association with hearing in noise performance by amplifying the aidable poorer ear in a repeated measures, longitudinal study.Design:The cross-sectional and longitudinal cohorts were comprised of 49 subjects (AHL; N = 21; 11 male, 10 female; mean age = 48 years) and NH (N = 28; 16 male, 12 female; mean age = 45 years). The maximum interaural threshold difference of the two cohorts spanned from 0 to 65 dB. Magnetoencephalography analyses focused on latency of the M100 peak response from auditory cortex in both hemispheres between 50 msec and 150 msec following monaural tonal stimulation at the frequency (0.5, 1, 2, 3, or 4 kHz) corresponding to the maximum and minimum interaural threshold difference for better and poorer ears separately. The longitudinal AHL cohort was drawn from three subjects in the cross-sectional AHL cohort (all male; ages 49 to 60 years; varied AHL etiologies; no amplification for at least 2 years). All longitudinal study subjects were treated by monaural amplification of the poorer ear and underwent repeated measures examination of the M100 response latency and quick speech in noise hearing in noise performance at baseline, and postamplification months 3, 6, and 12.Results:The M100 response peak latency values in the ipsilateral hemisphere lagged those in the contralateral hemisphere for all stimulation conditions. The mean (SD) interhemispheric latency difference values (ipsilateral less contralateral) to better ear stimulation for three categories of maximum interaural threshold difference were as follows: NH (≤ 10 dB)—8.6 (3.0) msec; AHL (15 to 40 dB)—3.0 (1.2) msec; AHL (≥ 45 dB)—1.4 (1.3) msec. In turn, the magnitude of difference values were used to define interhemispheric temporal organization states of asynchrony, mixed asynchrony and synchrony, and synchrony, respectively. Amplification of the poorer ear in longitudinal subjects drove interhemispheric organization change from baseline synchrony to postamplification asynchrony and hearing in noise performance improvement in those with baseline impairment over a 12-month period.Conclusions:Interhemispheric temporal organization in AHL was anchored between states of asynchrony in NH and synchrony in single-sided deafness. For asymmetry magnitudes between 15 and 40 dB, the intermediate mixed state of asynchrony and synchrony was continuous and reversible. Amplification of the poorer ear in AHL improved hearing in noise performance and restored normal temporal organization of auditory cortices in the two hemispheres. The return to normal interhemispheric asynchrony from baseline synchrony and improvement in hearing following monoaural amplification of the poorer ear evolved progressively over a 12-month period.

Mapping Specific Mental Content during Musical Imagery.

Humans can mentally represent auditory information without an external stimulus, but the specificity of these internal representations remains unclear. Here, we asked how similar the temporally unfolding neural representations of imagined music are compared to those during the original perceived experience. We also tested whether rhythmic motion can influence the neural representation of music during imagery as during perception. Participants first memorized six 1-min-long instrumental musical pieces with high accuracy. Functional MRI data were collected during: 1) silent imagery of melodies to the beat of a visual metronome; 2) same but while tapping to the beat; and 3) passive listening. During imagery, inter-subject correlation analysis showed that melody-specific temporal response patterns were reinstated in right associative auditory cortices. When tapping accompanied imagery, the melody-specific neural patterns were reinstated in more extensive temporal-lobe regions bilaterally. These results indicate that the specific contents of conscious experience are encoded similarly during imagery and perception in the dynamic activity of auditory cortices. Furthermore, rhythmic motion can enhance the reinstatement of neural patterns associated with the experience of complex sounds, in keeping with models of motor to sensory influences in auditory processing.

Humor and emotion: Quantitative meta analyses of functional neuroimaging studies

Humor is a ubiquitous aspect of human behavior that is infrequently the focus of neuroscience research. To localize human brain structures associated with the experience of humor, we conducted quantitative activation likelihood estimate (ALE) meta analyses of 57 fMRI studies (n = 1248) reporting enhanced regional brain activity evoked by humorous cues versus matched control cues. We performed separate ALE analyses of studies that employed picture-driven, text-based, and auditory laughter cues to evoke humor. A primary finding was that complex humor activates supramodal areas of the brain strongly associated with emotional processes, including bilateral amygdala and inferior frontal gyrus. Moreover, activation in brain regions associated with language, semantic knowledge, and theory of mind were differentially modulated by text and picture-driven humor cues, while hearing laughter enhances activation in auditory association cortex. The identification of humor-driven brain networks has the potential to expand brain-derived models of human emotion and could provide useful targets in translational research and therapy.

Extracellular voltage thresholds for maximizing information extraction in primate auditory cortex: implications for a brain computer interface

Objective. Research by Oby (2016 J. Neural. Eng. 13 036009) demonstrated that the optimal threshold for extracting information from visual and motor cortices may differ from the optimal threshold for identifying single neurons via spike sorting methods. The optimal threshold for extracting information from auditory cortex has yet to be identified, nor has the optimal temporal scale for representing auditory cortical activity. Here, we describe a procedure to jointly optimize the extracellular threshold and bin size with respect to the decoding accuracy achieved by a linear classifier for a diverse set of auditory stimuli. Approach. We used linear multichannel arrays to record extracellular neural activity from the auditory cortex of awake squirrel monkeys passively listening to both simple and complex sounds. We executed a grid search of the coordinate space defined by the voltage threshold (in units of standard deviation) and the bin size (in units of milliseconds), and computed decoding accuracy at each point. Main results. The optimal threshold for information extraction was consistently near two standard deviations below the voltage trace mean, which falls significantly below the range of three to five standard deviations typically used as inputs to spike sorting algorithms in basic research and in brain-computer interface (BCI) applications. The optimal binwidth was minimized at the optimal voltage threshold, particularly for acoustic stimuli dominated by temporally dynamic features, indicating that permissive thresholding permits readout of cortical responses with temporal precision on the order of a few milliseconds. Significance. The improvements in decoding accuracy we observed for optimal readout parameters suggest that standard thresholding methods substantially underestimate the information present in auditory cortical spiking patterns. The fact that optimal thresholds were relatively low indicates that local populations of cortical neurons exhibit high temporal coherence that could be leveraged in service of future auditory BCI applications.

Auditory cortex is susceptible to lexical influence as revealed by informational vs. energetic masking of speech categorization

Speech perception requires the grouping of acoustic information into meaningful phonetic units via the process of categorical perception (CP). Environmental masking influences speech perception and CP. However, it remains unclear at which stage of processing (encoding, decision, or both) masking affects listeners’ categorization of speech signals. The purpose of this study was to determine whether linguistic interference influences the early acoustic–phonetic conversion process inherent to CP. To this end, we measured source level, event related brain potentials (ERPs) from auditory cortex (AC) and inferior frontal gyrus (IFG) as listeners rapidly categorized speech sounds along a /da/ to /ga/ continuum presented in three listening conditions: quiet, and in the presence of forward (informational masker) and time-reversed (energetic masker) 2-talker babble noise. Maskers were matched in overall SNR and spectral content and thus varied only in their degree of linguistic interference (i.e., informational masking). We hypothesized a differential effect of informational versus energetic masking on behavioral and neural categorization responses, where we predicted increased activation of frontal regions when disambiguating speech from noise, especially during lexical-informational maskers. We found (1) informational masking weakens behavioral speech phoneme identification above and beyond energetic masking; (2) low-level AC activity not only codes speech categories but is susceptible to higher-order lexical interference; (3) identifying speech amidst noise recruits a cross hemispheric circuit (ACleft → IFGright) whose engagement varies according to task difficulty. These findings provide corroborating evidence for top-down influences on the early acoustic–phonetic analysis of speech through a coordinated interplay between frontotemporal brain areas.

Information diversity in individual auditory cortical neurons is associated with functionally distinct coordinated neuronal ensembles

Neuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.

Corticostriatal control of defense behavior in mice induced by auditory looming cues

Animals exhibit innate defense behaviors in response to approaching threats cued by the dynamics of sensory inputs of various modalities. The underlying neural circuits have been mostly studied in the visual system, but remain unclear for other modalities. Here, by utilizing sounds with increasing (vs. decreasing) loudness to mimic looming (vs. receding) objects, we find that looming sounds elicit stereotypical sequential defensive reactions: freezing followed by flight. Both behaviors require the activity of auditory cortex, in particular the sustained type of responses, but are differentially mediated by corticostriatal projections primarily innervating D2 neurons in the tail of the striatum and corticocollicular projections to the superior colliculus, respectively. The behavioral transition from freezing to flight can be attributed to the differential temporal dynamics of the striatal and collicular neurons in their responses to looming sound stimuli. Our results reveal an essential role of the striatum in the innate defense control.

Neuroplastic changes in auditory cortex induced by long-duration “non-traumatic” noise exposures are triggered by deficits in the neural output of the cochlea

Long-term exposure to moderate intensity noise that does not cause measureable hearing loss can cause striking changes in sound-evoked neural activity in auditory cortex. It is unclear if these changes originate in the cortex or result from functional deficits in the neural output of the cochlea. To explore this issue, rats were exposed for 6-weeks to 18–24 kHz noise at 45, 65 or 85 dB SPL and then compared the noise-induced changes in the cochlear compound action potential (CAP) with the neurophysiological alterations in the anterior auditory field (AAF) of auditory cortex. The 45-dB exposure, which had no effect on the cochlear CAP also had no effect on the AAF. In contrast, the 85-dB exposure greatly reduced CAP amplitudes at high frequencies, but had little or no effect on low frequencies. Despite the large reduction in high-frequency CAP neural responses, high frequency AAF neural responses (spike rate and local field potential amplitude) remained largely within normal limits, evidence of central gain compensation. AAF responses were also enhanced at the low frequencies even though CAP responses were normal; this AAF hyperactivity only occurred at low-moderate intensities (level-dependent enhanced central gain). The 65-dB exposure also caused a moderate reduction in high-frequency CAP amplitudes. Notwithstanding this cochlear loss, AAF responses were boosted into the normal range, evidence of homeostatic gain compensation. Our results suggest that the noise-induced neuroplastic changes in the auditory cortex from so-called “non-traumatic” exposures are triggered from functional deficits in the neural output of the cochlea.