Neural Activity In Auditory Cortex Research Articles

A neural signature of regularity in sound is reduced in older adults

Sensitivity to repetitions in sound amplitude and frequency is crucial for sound perception. As with other aspects of sound processing, sensitivity to such patterns may change with age, and may help explain some age-related changes in hearing such as segregating speech from background sound. We recorded magnetoencephalography to characterize differences in the processing of sound patterns between younger and older adults. We presented tone sequences that either contained a pattern (made of a repeated set of tones) or did not contain a pattern. We show that auditory cortex in older, compared to younger, adults is hyperresponsive to sound onsets, but that sustained neural activity in auditory cortex, indexing the processing of a sound pattern, is reduced. Hence, the sensitivity of neural populations in auditory cortex fundamentally differs between younger and older individuals, overresponding to sound onsets, while underresponding to patterns in sounds. This may help to explain some age-related changes in hearing such as increased sensitivity to distracting sounds and difficulties tracking speech in the presence of other sound.

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.

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.

Auditory cortex activity related to perceptual awareness versus masking of tone sequences

Sequences of repeating tones can be masked by other tones of different frequency. When these tone sequences are perceived, nevertheless, a prominent neural response in the auditory cortex is evoked by each tone of the sequence. When the targets are detected based on their isochrony, participants know that they are listening to the target once they detected it. To explore if the neural activity is more closely related to this detection task or to perceptual awareness, this magnetoencephalography (MEG) study used targets that could only be identified with cues provided after or before the masked target. In experiment 1, multiple mono-tone streams with jittered inter-stimulus interval were used, and the tone frequency of the target was indicated by a cue. Results showed no differential auditory cortex activity between hit and miss trials with post-stimulus cues. A late negative response for hit trials was only observed for pre-stimulus cues, suggesting a task-related component. Since experiment 1 provided no evidence for a link of a difference response with tone awareness, experiment 2 was planned to probe if detection of tone streams was linked to a difference response in auditory cortex. Random-tone sequences were presented in the presence of a multi-tone masker, and the sequence was repeated without masker thereafter. Results showed a prominent difference wave for hit compared to miss trials in experiment 2 evoked by targets in the presence of the masker. These results suggest that perceptual awareness of tone streams is linked to neural activity in auditory cortex.

Learning boosts the decoding of sound sequences in rat auditory cortex.

Continuous acoustic streams, such as speech signals, can be chunked into segments containing reoccurring patterns (e.g., words). Noninvasive recordings of neural activity in humans suggest that chunking is underpinned by low-frequency cortical entrainment to the segment presentation rate, and modulated by prior segment experience (e.g., words belonging to a familiar language). Interestingly, previous studies suggest that also primates and rodents may be able to chunk acoustic streams. Here, we test whether neural activity in the rat auditory cortex is modulated by previous segment experience. We recorded subdural responses using electrocorticography (ECoG) from the auditory cortex of 11 anesthetized rats. Prior to recording, four rats were trained to detect familiar triplets of acoustic stimuli (artificial syllables), three were passively exposed to the triplets, while another four rats had no training experience. While low-frequency neural activity peaks were observed at the syllable level, no triplet-rate peaks were observed. Notably, in trained rats (but not in passively exposed and naïve rats), familiar triplets could be decoded more accurately than unfamiliar triplets based on neural activity in the auditory cortex. These results suggest that rats process acoustic sequences, and that their cortical activity is modulated by the training experience even under subsequent anesthesia.

Multi-sensory Gamma Stimulation Ameliorates Alzheimer’s-Associated Pathology and Improves Cognition

We previously reported that inducing gamma oscillations with a non-invasive light flicker (gamma entrainment using sensory stimulus or GENUS) impacted pathology in the visual cortex of Alzheimer's disease mouse models. Here, we designed auditory tone stimulation that drove gamma frequency neural activity in auditory cortex (AC) and hippocampal CA1. Seven days of auditory GENUS improved spatial and recognition memory and reduced amyloid in AC and hippocampus of 5XFAD mice. Changes in activation responses were evident in microglia, astrocytes, and vasculature. Auditory GENUS also reduced phosphorylated tau in the P301S tauopathy model. Furthermore, combined auditory and visual GENUS, but not either alone, produced microglial-clustering responses, and decreased amyloid in medial prefrontal cortex. Whole brain analysis using SHIELD revealed widespread reduction of amyloid plaques throughout neocortex after multi-sensory GENUS. Thus, GENUS can be achieved through multiple sensory modalities with wide-ranging effects across multiple brain areas to improve cognitive function.

Sound identity is represented robustly in auditory cortex during perceptual constancy

Perceptual constancy requires neural representations that are selective for object identity, but also tolerant across identity-preserving transformations. How such representations arise in the brain and support perception remains unclear. Here, we study tolerant representation of sound identity in the auditory system by recording neural activity in auditory cortex of ferrets during perceptual constancy. Ferrets generalize vowel identity across variations in fundamental frequency, sound level and location, while neurons represent sound identity robustly across acoustic variations. Stimulus features are encoded with distinct time-courses in all conditions, however encoding of sound identity is delayed when animals fail to generalize and during passive listening. Neurons also encode information about task-irrelevant sound features, as well as animals’ choices and accuracy, while population decoding out-performs animals’ behavior. Our results show that during perceptual constancy, sound identity is represented robustly in auditory cortex across widely varying conditions, and behavioral generalization requires conserved timing of identity information.

The time course of contextual cohort effects in auditory processing of category-ambiguous words: MEG evidence for a single “clash” as noun or verb

ABSTRACTThe size and probability distribution of a word-form’s cohort of lexical competitors influence auditory processing and can be constrained by syntactic category information. This experiment employs noun/verb homonyms (e.g. “ache”) presented in syntactic context to clarify the mechanisms and representations involved in context-based cohort restriction. Implications for theories positing single versus multiple word-forms in cases of category ambiguity also arise. Using correlations between neural activity in auditory cortex, measured by magnetoencephalography (MEG), and standard and context-dependent cohort entropy and phoneme surprisal variables, we consider the possibility of cohort restriction on the basis of form or on the basis of category usage. Crucially, the form-conditional measure is consistent only with a single word-form view of category ambiguity. Our results show that noun/verb homonyms are derived from single category-neutral word-forms and that the cohort is restricted incrementally in context, by form and then by usage.

Contributions of sensory tuning to auditory-vocal interactions in marmoset auditory cortex

During speech, humans continuously listen to their own vocal output to ensure accurate communication. Such self-monitoring is thought to require the integration of information about the feedback of vocal acoustics with internal motor control signals. The neural mechanism of this auditory-vocal interaction remains largely unknown at the cellular level. Previous studies in naturally vocalizing marmosets have demonstrated diverse neural activities in auditory cortex during vocalization, dominated by a vocalization-induced suppression of neural firing. How underlying auditory tuning properties of these neurons might contribute to this sensory-motor processing is unknown. In the present study, we quantitatively compared marmoset auditory cortex neural activities during vocal production with those during passive listening. We found that neurons excited during vocalization were readily driven by passive playback of vocalizations and other acoustic stimuli. In contrast, neurons suppressed during vocalization exhibited more diverse playback responses, including responses that were not predictable by auditory tuning properties. These results suggest that vocalization-related excitation in auditory cortex is largely a sensory-driven response. In contrast, vocalization-induced suppression is not well predicted by a neuron's auditory responses, supporting the prevailing theory that internal motor-related signals contribute to the auditory-vocal interaction observed in auditory cortex.

A cortical-hippocampal-cortical loop of information processing during memory consolidation.

Hippocampal replay during sharp-wave ripple events (SWRs) is thought to drive memory consolidation in hippocampal and cortical circuits. Changes in neocortical activity can precede SWR events, but whether and how these changes influence the content of replay remains unknown. Here we show that during sleep there is a rapid cortical-hippocampal-cortical loop of information flow around the times of SWRs. We recorded neural activity in auditory cortex (AC) and hippocampus of rats as they learned a sound-guided task and during sleep. We found that patterned activation in AC precedes and predicts the subsequent content of hippocampal activity during SWRs, while hippocampal patterns during SWRs predict subsequent AC activity. Delivering sounds during sleep biased AC activity patterns, and sound-biased AC patterns predicted subsequent hippocampal activity. These findings suggest that activation of specific cortical representations during sleep influences the identity of the memories that are consolidated into long-term stores.

Persistent neural activity in auditory cortex is related to auditory working memory in humans and nonhuman primates.

Working memory is the cognitive capacity of short-term storage of information for goal-directed behaviors. Where and how this capacity is implemented in the brain are unresolved questions. We show that auditory cortex stores information by persistent changes of neural activity. We separated activity related to working memory from activity related to other mental processes by having humans and monkeys perform different tasks with varying working memory demands on the same sound sequences. Working memory was reflected in the spiking activity of individual neurons in auditory cortex and in the activity of neuronal populations, that is, in local field potentials and magnetic fields. Our results provide direct support for the idea that temporary storage of information recruits the same brain areas that also process the information. Because similar activity was observed in the two species, the cellular bases of some auditory working memory processes in humans can be studied in monkeys.

Decoding Visual Location From Neural Patterns in the Auditory Cortex of the Congenitally Deaf

Sensory cortices of individuals who are congenitally deprived of a sense can exhibit considerable plasticity and be recruited to process information from the senses that remain intact. Here, we explored whether the auditory cortex of congenitally deaf individuals represents visual field location of a stimulus—a dimension that is represented in early visual areas. We used functional MRI to measure neural activity in auditory and visual cortices of congenitally deaf and hearing humans while they observed stimuli typically used for mapping visual field preferences in visual cortex. We found that the location of a visual stimulus can be successfully decoded from the patterns of neural activity in auditory cortex of congenitally deaf but not hearing individuals. This is particularly true for locations within the horizontal plane and within peripheral vision. These data show that the representations stored within neuroplastically changed auditory cortex can align with dimensions that are typically represented in visual cortex.

Chapter 5 - Temporal coding in the auditory cortex

Speech is a complex acoustic signal showing a quasiperiodic structure at several timescales. Integrated neural signals recorded in the cortex also show periodicity at different timescales. In this chapter we outline the neural mechanisms that potentially allow the auditory cortex to segment and encode continuous speech. This chapter focuses on how the human auditory cortex uses the temporal structure of the acoustic signal to extract phonemes and syllables, the two major constituents of connected speech. We argue that the quasiperiodic structure of collective neural activity in auditory cortex represents the ideal mechanical infrastructure to fractionate continuous speech into linguistic constituents of variable sizes.

A novel behavioral assay for the assessment of acute tinnitus in rats optimized for simultaneous recording of oscillatory neural activity

BackgroundHuman magneto/electrophysiology studies suggest that the phantom sound of tinnitus arises from spontaneous oscillatory neural activity in auditory cortex; however, in animal models, behavioral techniques suitable for testing this hypothesis in combination with electrophysiology recordings have yet to be evaluated. While electrophysiological studies of tinnitus have been reported in passive, awake animals, these studies fail to control for attentional mechanisms likely to play a role in the perception of tinnitus. New methodA novel appetitive operant conditioning, two-alternative identification task was developed for detecting acute tinnitus in rats. The procedure optimizes conditions for simultaneously recording oscillatory neural activity while controlling for the attentional state of the animal. ResultsTinnitus was detected in six of seven rats following systemic injection with sodium salicylate (200mg/kg IP), a known inducer of tinnitus. Analysis of ongoing local field potentials recorded from chronically implanted electrodes in auditory cortex of a rat reporting tinnitus revealed changes in the spectrum of ongoing neural activity.Comparison with existing method(s): Existing tinnitus-detection methods were not explicitly designed for the simultaneous recording of neural activity. The behavioral method reported here is the first to provide the conditions necessary for obtaining these recordings in chronically implanted rats. ConclusionsThe behavioral assay presented here will facilitate research into the neural mechanisms of tinnitus by allowing researchers to compare the electrophysiological data in animals with confirmed tinnitus.

Feedback that confirms reward expectation triggers auditory cortex activity

Associative learning studies have shown that the anticipation of reward and punishment shapes the representation of sensory stimuli, which is further modulated by dopamine. Less is known about whether and how reward delivery activates sensory cortices and the role of dopamine at that time point of learning. We used an appetitive instrumental learning task in which participants had to learn that a specific class of frequency-modulated tones predicted a monetary reward following fast and correct responses in a succeeding reaction time task. These fMRI data were previously analyzed regarding the effect of reward anticipation, but here we focused on neural activity to the reward outcome relative to the reward expectation and tested whether such activation in the reward reception phase is modulated by L-DOPA. We analyzed neural responses at the time point of reward outcome under three different conditions: 1) when a reward was expected and received, 2) when a reward was expected but not received, and 3) when a reward was not expected and not received. Neural activity in auditory cortex was enhanced during feedback delivery either when an expected reward was received or when the expectation of obtaining no reward was correct. This differential neural activity in auditory cortex was only seen in subjects who learned the reward association and not under dopaminergic modulation. Our data provide evidence that auditory cortices are active at the time point of reward outcome. However, responses are not dependent on the reward itself but on whether the outcome confirmed the subject's expectations.

Positive and negative reinforcement activate human auditory cortex.

Prior studies suggest that reward modulates neural activity in sensory cortices, but less is known about punishment. We used functional magnetic resonance imaging and an auditory discrimination task, where participants had to judge the duration of frequency modulated tones. In one session correct performance resulted in financial gains at the end of the trial, in a second session incorrect performance resulted in financial loss. Incorrect performance in the rewarded as well as correct performance in the punishment condition resulted in a neutral outcome. The size of gains and losses was either low or high (10 or 50 Euro cent) depending on the direction of frequency modulation. We analyzed neural activity at the end of the trial, during reinforcement, and found increased neural activity in auditory cortex when gaining a financial reward as compared to gaining no reward and when avoiding financial loss as compared to receiving a financial loss. This was independent on the size of gains and losses. A similar pattern of neural activity for both gaining a reward and avoiding a loss was also seen in right middle temporal gyrus, bilateral insula and pre-supplemental motor area, here however neural activity was lower after correct responses compared to incorrect responses. To summarize, this study shows that the activation of sensory cortices, as previously shown for gaining a reward is also seen during avoiding a loss.

Effects of L-dopa during auditory instrumental learning in humans.

The dopaminergic neurotransmitter system is critically involved in promoting plasticity in auditory cortex. We combined functional magnetic resonance imaging (fMRI) and a pharmacological manipulation to investigate dopaminergic modulation of neural activity in auditory cortex during instrumental learning. Volunteers either received 100 mg L-dopa (Madopar) or placebo in an appetitive, differential instrumental conditioning paradigm, which involved learning that a specific category of frequency modulated tones predicts a monetary reward when fast responses were made in a subsequent reaction time task. The other category of frequency modulated tones was not related to a reward. Our behavioral data provides evidence that dopaminergic stimulation differentially impacts on the speed of instrumental responding in rewarded and unrewarded trials. L-dopa increased neural BOLD activity in left auditory cortex to tones in rewarded and unrewarded trials. This increase was related to plasma L-dopa levels and learning rate. Our data thus provides evidence for dopaminergic modulation of neural activity in auditory cortex, which occurs for both auditory stimuli related to a later reward and those not related to a reward.

Neural Correlates of the Lombard Effect in Primate Auditory Cortex

Speaking is a sensory-motor process that involves constant self-monitoring to ensure accurate vocal production. Self-monitoring of vocal feedback allows rapid adjustment to correct perceived differences between intended and produced vocalizations. One important behavior in vocal feedback control is a compensatory increase in vocal intensity in response to noise masking during vocal production, commonly referred to as the Lombard effect. This behavior requires mechanisms for continuously monitoring auditory feedback during speaking. However, the underlying neural mechanisms are poorly understood. Here we show that when marmoset monkeys vocalize in the presence of masking noise that disrupts vocal feedback, the compensatory increase in vocal intensity is accompanied by a shift in auditory cortex activity toward neural response patterns seen during vocalizations under normal feedback condition. Furthermore, we show that neural activity in auditory cortex during a vocalization phrase predicts vocal intensity compensation in subsequent phrases. These observations demonstrate that the auditory cortex participates in self-monitoring during the Lombard effect, and may play a role in the compensation of noise masking during feedback-mediated vocal control.

Beyond auditory cortex: working with musical thoughts

Musical imagery is associated with neural activity in auditory cortex, but prior studies have not examined musical imagery tasks requiring mental transformations. This paper describes functional magnetic resonance imaging (fMRI) studies requiring manipulation of musical information. In one set of experiments, listeners were asked to mentally reverse a familiar tune when presented backwards. This manipulation consistently elicits neural activity in the intraparietal sulcus (IPS). Separate experiments requiring judgments about melodies that have been transposed from one musical key to another also elicit IPS activation. Conjunction analyses indicate that the same portions of the IPS are recruited in both tasks. The findings suggest that the dorsal pathway of auditory processing is involved in the manipulation and transformation of auditory information, as has also been shown for visuomotor and visuospatial tasks. As such, it provides a substrate for the creation of new mental representations that are based on manipulation of previously experienced sensory events.

Altered Neural Responses to Sounds in Primate Primary Auditory Cortex during Slow-Wave Sleep

How sounds are processed by the brain during sleep is an important question for understanding how we perceive the sensory environment in this unique behavioral state. While human behavioral data have indicated selective impairments of sound processing during sleep, brain imaging and neurophysiology studies have reported that overall neural activity in auditory cortex during sleep is surprisingly similar to that during wakefulness. This responsiveness to external stimuli leaves open the question of how neural responses during sleep differ, if at all, from wakefulness. Using extracellular neural recordings in the primary auditory cortex of naturally sleeping common marmosets, we show that slow-wave sleep (SWS) alters neural responses in the primate auditory cortex in two specific ways. SWS reduced the sensitivity of auditory cortex such that quiet sounds elicited weak responses in SWS compared with wakefulness, while loud sounds evoked similar responses in SWS and wakefulness. Furthermore, SWS reduced the extent of sound-evoked response suppression. This pattern of alterations was not observed during rapid eye movement sleep and could not be easily explained by the presence of slow rhythms in SWS. The alteration of excitatory and inhibitory responses during SWS suggests limitations in auditory processing and provides novel insights for understanding why certain sounds are processed while others are missed during deep sleep.