Cross-frequency coupling in cortico-hippocampal networks supports the maintenance of sequential auditory information in short-term memory.

It has been suggested that cross-frequency coupling in cortico-hippocampal networks enables the maintenance of multiple visuo-spatial items in working memory. However, whether this mechanism acts as a global neural code for memory retention across sensory modalities remains to be demonstrated. Intracranial EEG data were recorded while drug-resistant patients with epilepsy performed a delayed matched-to-sample task with tone sequences. We manipulated task difficulty by varying the memory load and the duration of the silent retention period between the to-be-compared sequences. We show that the strength of theta-gamma phase amplitude coupling in the superior temporal sulcus, the inferior frontal gyrus, the inferior temporal gyrus, and the hippocampus (i) supports the short-term retention of auditory sequences; (ii) decodes correct and incorrect memory trials as revealed by machine learning analysis; and (iii) is positively correlated with individual short-term memory performance. Specifically, we show that successful task performance is associated with consistent phase coupling in these regions across participants, with gamma bursts restricted to specific theta phase ranges corresponding to higher levels of neural excitability. These findings highlight the role of cortico-hippocampal activity in auditory short-term memory and expand our knowledge about the role of cross-frequency coupling as a global biological mechanism for information processing, integration, and memory in the human brain.

Neurocomputational Underpinnings of Expected Surprise.

Predictive coding accounts of brain functions profoundly influence current approaches to perceptual synthesis. However, a fundamental paradox has emerged, that may be very relevant for understanding hallucinations, psychosis, or cognitive inflexibility: in some situations, surprise or prediction error-related responses can decrease when predicted, and yet, they can increase when we know they are predictable. This paradox is resolved by recognizing that brain responses reflect precision-weighted prediction error. This presses us to disambiguate the contributions of precision and prediction error in electrophysiology. To meet this challenge for the first time, we appeal to a methodology that couples an original experimental paradigm with fine dynamic modeling. We examined brain responses in healthy human participants (N = 20; 10 female) to unexpected and expected surprising sounds, assuming that the latter yield a smaller prediction error but much more amplified by a larger precision weight. Importantly, addressing this modulation requires the modeling of trial-by-trial variations of brain responses, that we reconstructed within a fronto-temporal network by combining EEG and MEG. Our results reveal an adaptive learning of surprise with larger integration of past (relevant) information in the context of expected surprises. Within the auditory hierarchy, this adaptation was found tied down to specific connections and reveals in particular precision encoding through neuronal excitability. Strikingly, these fine processes are automated as sound sequences were unattended. These findings directly speak to applications in psychiatry, where specifically impaired precision weighting has been suggested to be at the heart of several conditions such as schizophrenia and autism.SIGNIFICANCE STATEMENT In perception as Bayesian inference and learning, context sensitivity expresses as the precision weighting of prediction errors. A subtle mechanism that is thought to lie at the heart of several psychiatric conditions. It is thus critical to identify its neurophysiological and computational underpinnings. We revisit the passive auditory oddball paradigm by manipulating sound predictability and use a twofold modeling approach to simultaneous EEG-MEG recordings: (1) trial-by-trial modeling of cortical responses reveals a context-sensitive perceptual learning process; (2) the dynamic causal modeling (DCM) of evoked responses uncovers the associated changes in synaptic efficacy. Predictability discloses a link between precision weighting and self-inhibition of superficial pyramidal (SP) cells, a result that paves the way to a fine description of healthy and pathologic perception.

Consonance Perception in Congenital Amusia: Behavioral and Brain Responses to Harmonicity and Beating Cues.

Congenital amusia is a neurodevelopmental disorder characterized by difficulties in the perception and production of music, including the perception of consonance and dissonance, or the judgment of certain combinations of pitches as more pleasant than others. Two perceptual cues for dissonance are inharmonicity (the lack of a common fundamental frequency between components) and beating (amplitude fluctuations produced by close, interacting frequency components). Amusic individuals have previously been reported to be insensitive to inharmonicity, but to exhibit normal sensitivity to beats. In the present study, we measured adaptive discrimination thresholds in amusic participants and found elevated thresholds for both cues. We recorded EEG and measured the MMN in evoked potentials to consonance and dissonance deviants in an oddball paradigm. The amplitude of the MMN response was similar overall for amusic and control participants; however, in controls, there was a tendency toward larger MMNs for inharmonicity than for beating cues, whereas the opposite tendency was observed for the amusic participants. These findings suggest that initial encoding of consonance cues may be intact in amusia despite impaired behavioral performance, but that the relative weight of nonspectral (beating) cues may be increased for amusic individuals.

Individuals with congenital amusia remember music they like.

Music is better recognized when it is liked. Does this association remain evident when music perception and memory are severely impaired, as in congenital amusia? We tested 11 amusic and 11 matched control participants, asking whether liking of a musical excerpt influences subsequent recognition. In an initial exposure phase, participants-unaware that their recognition would be tested subsequently-listened to 24 musical excerpts and judged how much they liked each excerpt. In the test phase that followed, participants rated whether they recognized the previously heard excerpts, which were intermixed with an equal number of foils matched for mode, tempo, and musical genre. As expected, recognition was in general impaired for amusic participants compared with control participants. For both groups, however, recognition was better for excerpts that were liked, and the liking enhancement did not differ between groups. These results contribute to a growing body of research that examines the complex interplay between emotions and cognitive processes. More specifically, they extend previous findings related to amusics' impairments to a new memory paradigm and suggest that (1) amusic individuals are sensitive to an aesthetic and subjective dimension of the music-listening experience, and (2) emotions can support memory processes even in a population with impaired music perception and memory.

Age-related differences in bottom-up and top-down attention: Insights from EEG and MEG.

Attention operates through top-down and bottom-up processes, and a balance between these processes is crucial for daily tasks. Imperilling such balance could explain ageing-associated attentional problems such as exacerbated distractibility. In this study, we aimed to characterize this enhanced distractibility by investigating the impact of ageing upon event-related components associated with top-down and bottom-up attentional processes. MEG and EEG data were acquired from 14 older and 14 younger healthy adults while performing a task that conjointly evaluates top-down and bottom-up attention. Event-related components were analysed on sensor and source levels. In comparison with the younger group, the older mainly displayed (1) reduced target anticipation processes (reduced CMV), (2) increased early target processing (larger P50 but smaller N1) and (3) increased processing of early distracting sounds (larger N1 but reduced P3a), followed by a (4) prolonged reorientation towards the main task (larger RON). Taken together, our results suggest that the enhanced distractibility in ageing could stem from top-down deficits, in particular from reduced inhibitory and reorientation processes.

Enhanced mismatch negativity in harmonic compared with inharmonic sounds.

Many natural sounds have frequency spectra composed of integer multiples of a fundamental frequency. This property, known as harmonicity, plays an important role in auditory information processing. However, the extent to which harmonicity influences the processing of sound features beyond pitch is still unclear. This is interesting because harmonic sounds have lower information entropy than inharmonic sounds. According to predictive processing accounts of perception, this property could produce more salient neural responses due to the brain's weighting of sensory signals according to their uncertainty. In the present study, we used electroencephalography to investigate brain responses to harmonic and inharmonic sounds commonly occurring in music: Piano tones and hi-hat cymbal sounds. In a multifeature oddball paradigm, we measured mismatch negativity (MMN) and P3a responses to timbre, intensity, and location deviants in listeners with and without congenital amusia-an impairment of pitch processing. As hypothesized, we observed larger amplitudes and earlier latencies (for both MMN and P3a) in harmonic compared with inharmonic sounds. These harmonicity effects were modulated by sound feature. Moreover, the difference in P3a latency between harmonic and inharmonic sounds was larger for controls than amusics. We propose an explanation of these results based on predictive coding and discuss the relationship between harmonicity, information entropy, and precision weighting of prediction errors.

Dream recall frequency is associated with attention rather than with working memory abilities.

Several factors influencing dream recall frequency (DRF) have been identified, but some remain poorly understood. One way to study DRF is to compare cognitive processes in low and high dream recallers (LR and HR). According to the arousal-retrieval model, long-term memory encoding of a dream requires wakefulness while its multisensory short-term memory is still alive. Previous studies showed contradictory results concerning short-term memory differences between LR and HR. It has also been found that extreme DRFs are associated with different electrophysiological traits related to attentional processes. However, to date, there is no evidence for attentional differences between LR and HR at the behavioural level. To further investigate attention and working memory in HR and LR, we used a newly-developed challenging paradigm called "MEMAT" (for MEMory and ATtention), which allows the study of selective attention and working memory interaction during memory encoding of non-verbal auditory stimuli. We manipulated the difficulties of the distractor to ignore and of the memory task. The performance of the two groups were not differentially impacted by working memory load. However, HR were slower and less accurate in the presence of a hard rather than easy to-ignore distractor, while LR were much less impacted by the distractor difficulty. Therefore, we show behavioural evidence towards less resistance to hard-to-ignore distractors in HR. Using a challenging task, we show for the first time, attentional differences between HR and LR at the behavioural level. The impact of auditory attention and working memory on dream recall is discussed.

Development of auditory cognition in 5- to 10-year-old children: Focus on musical and verbal short-term memory.

Developmental aspects of auditory cognition were investigated in 5-to-10-year-old children (n = 100). Musical and verbal short-term memory (STM) were assessed by means of delayed matching-to-sample tasks (DMST) (comparison of two four-item sequences separated by a silent retention delay), with two levels of difficulty. For musical and verbal materials, children's performance increased from 5 years to about 7 years of age, then remained stable up to 10 years of age, with performance remaining inferior to performance of young adults. Children and adults performed better with verbal material than with musical material. To investigate auditory cognition beyond STM, we assessed speech-in-noise perception with a four-alternative forced-choice task with two conditions of phonological difficulty and two levels of cocktail-party noise intensity. Partial correlations, factoring out the effect of age, showed a significant link between musical STM and speech-in-noise perception in the condition with increased noise intensity. Our findings reveal that auditory STM improves over development with a critical phase around 6-7 years of age, yet these abilities appear to be still immature at 10 years. Musical and verbal STM might in particular share procedural and serial order processes. Furthermore, musical STM and the ability to perceive relevant speech signals in cocktail-party noise might rely on shared cognitive resources, possibly related to pitch encoding. To the best of our knowledge, this is the first time that auditory STM is assessed with the same paradigm for musical and verbal material during childhood, providing perspectives regarding diagnosis and remediation in developmental learning disorders.

Tonal structures benefit short-term memory for real music: Evidence from non-musicians and individuals with congenital amusia.

Congenital amusia is a neurodevelopmental disorder of music processing, which includes impaired pitch memory, associated to abnormalities in the right fronto-temporal network. Previous research has shown that tonal structures (as defined by the Western musical system) improve short-term memory performance for short tone sequences (in comparison to atonal versions) in non-musician listeners, but the tonal structures only benefited response times in amusic individuals. We here tested the potential benefit of tonal structures for short-term memory with more complex musical material. Congenital amusics and their matched non-musician controls were required to indicate whether two excerpts were the same or different. Results confirmed impaired performance of amusic individuals in this short-term memory task. However, most importantly, both groups of participants showed better memory performance for tonal material than for atonal material. These results revealed that even amusics' impaired short-term memory for pitch shows classical characteristics of short-term memory, that is the mnemonic benefit of structure in the to-be-memorized material. The findings show that amusic individuals have acquired some implicit knowledge of regularities of their culture, allowing for implicit processing of tonal structures, which benefits to memory even for complex material.

Auditory and visual short-term memory: influence of material type, contour, and musical expertise.

Short-term memory has mostly been investigated with verbal or visuospatial stimuli and less so with other categories of stimuli. Moreover, the influence of sensory modality has been explored almost solely in the verbal domain. The present study compared visual and auditory short-term memory for different types of materials, aiming to understand whether sensory modality and material type can influence short-term memory performance. Furthermore, we aimed to assess if music expertise can modulate memory performance, as previous research has reported better auditory memory (and to some extent, visual memory), and better auditory contour recognition for musicians than non-musicians. To do so, we adapted the same recognition paradigm (delayed-matching to sample) across different types of stimuli. In each trial, participants (musicians and non-musicians) were presented with two sequences of events, separated by a silent delay, and had to indicate whether the two sequences were identical or different. The performance was compared for auditory and visual materials belonging to three different categories: (1) verbal (i.e., syllables); (2) nonverbal (i.e., that could not be easily denominated) with contour (based on loudness or luminance variations); and (3) nonverbal without contour (pink noise sequences or kanji letters sequences). Contour and no-contour conditions referred to whether the sequence can entail (or not) a contour (i.e., a pattern of up and down changes) based on non-pitch features. Results revealed a selective advantage of musicians for auditory no-contour stimuli and for contour stimuli (both visual and auditory), suggesting that musical expertise is associated with specific short-term memory advantages in domains close to the trained domain, also extending cross-modally when stimuli have contour information. Moreover, our results suggest a role of encoding strategies (i.e., how the material is represented mentally during the task) for short-term-memory performance.

Empirical Bayes evaluation of fused EEG-MEG source reconstruction: Application to auditory mismatch evoked responses.

We here turn the general and theoretical question of the complementarity of EEG and MEG for source reconstruction, into a practical empirical one. Precisely, we address the challenge of evaluating multimodal data fusion on real data. For this purpose, we build on the flexibility of Parametric Empirical Bayes, namely for EEG-MEG data fusion, group level inference and formal hypothesis testing. The proposed approach follows a two-step procedure by first using unimodal or multimodal inference to derive a cortical solution at the group level; and second by using this solution as a prior model for single subject level inference based on either unimodal or multimodal data. Interestingly, for inference based on the same data (EEG, MEG or both), one can then formally compare, as alternative hypotheses, the relative plausibility of the two unimodal and the multimodal group priors. Using auditory data, we show that this approach enables to draw important conclusions, namely on (i) the superiority of multimodal inference, (ii) the greater spatial sensitivity of MEG compared to EEG, (iii) the ability of EEG data alone to source reconstruct temporal lobe activity, (iv) the usefulness of EEG to improve MEG based source reconstruction. Importantly, we largely reproduce those findings over two different experimental conditions. We here focused on Mismatch Negativity (MMN) responses for which generators have been extensively investigated with little homogeneity in the reported results. Our multimodal inference at the group level revealed spatio-temporal activity within the supratemporal plane with a precision which, to our knowledge, has never been achieved before with non-invasive recordings.

Is Migraine Associated to Brain Anatomical Alterations? New Data and Coordinate-Based Meta-analysis.

A growing number of studies investigate brain anatomy in migraine using voxel- (VBM) and surface-based morphometry (SBM), as well as diffusion tensor imaging (DTI). The purpose of this article is to identify consistent patterns of anatomical alterations associated with migraine. First, 19 migraineurs without aura and 19 healthy participants were included in a brain imaging study. T1-weighted MRIs and DTI sequences were acquired and analyzed using VBM, SBM and tract-based spatial statistics. No significant alterations of gray matter (GM) volume, cortical thickness, cortical gyrification, sulcus depth and white-matter tract integrity could be observed. However, migraineurs displayed decreased white matter (WM) volume in the left superior longitudinal fasciculus. Second, a systematic review of the literature employing VBM, SBM and DTI was conducted to investigate brain anatomy in migraine. Meta-analysis was performed using Seed-based d Mapping via permutation of subject images (SDM-PSI) on GM volume, WM volume and cortical thickness data. Alterations of GM volume, WM volume, cortical thickness or white-matter tract integrity were reported in 72%, 50%, 56% and 33% of published studies respectively. Spatial distribution and direction of the disclosed effects were highly inconsistent across studies. The SDM-PSI analysis revealed neither significant decrease nor significant increase of GM volume, WM volume or cortical thickness in migraine. Overall there is to this day no strong evidence of specific brain anatomical alterations reliably associated to migraine. Possible explanations of this conflicting literature are discussed. Trial registration number: NCT02791997, registrated February 6th, 2015.

Correction to: A case of verbal and emotional prosody processing dissociation after a right temporal venous infarct.

The above article was published online with missing authors.

Specialized neural dynamics for verbal and tonal memory: fMRI evidence in congenital amusia.

Behavioral and neuropsychological studies have suggested that tonal and verbal short-term memory are supported by specialized neural networks. To date however, neuroimaging investigations have failed to confirm this hypothesis. In this study, we investigated the hypothesis of distinct neural resources for tonal and verbal memory by comparing typical nonmusician listeners to individuals with congenital amusia, who exhibit pitch memory impairments with preserved verbal memory. During fMRI, amusics and matched controls performed delayed-match-to-sample tasks with tones and words and perceptual control tasks with the same stimuli. For tonal maintenance, amusics showed decreased activity in the right auditory cortex, inferior frontal gyrus (IFG) and dorso-lateral-prefrontal cortex (DLPFC). Moreover, they exhibited reduced right-lateralized functional connectivity between the auditory cortex and the IFG during tonal encoding and between the IFG and the DLPFC during tonal maintenance. In contrasts, amusics showed no difference compared with the controls for verbal memory, with activation in the left IFG and left fronto-temporal connectivity. Critically, we observed a group-by-material interaction in right fronto-temporal regions: while amusics recruited these regions less strongly for tonal memory than verbal memory, control participants showed the reversed pattern (tonal > verbal). By benefitting from the rare condition of amusia, our findings suggest specialized cortical systems for tonal and verbal short-term memory in the human brain.

Short- and long-term memory for pitch and non-pitch contours: Insights from congenital amusia.

Congenital amusia is a neurodevelopmental disorder characterized by deficits in music perception, including discriminating and remembering melodies and melodic contours. As non-amusic listeners can perceive contours in dimensions other than pitch, such as loudness and brightness, our present study investigated whether amusics' pitch contour deficits also extend to these other auditory dimensions. Amusic and control participants performed an identification task for ten familiar melodies and a short-term memory task requiring the discrimination of changes in the contour of novel four-tone melodies. For both tasks, melodic contour was defined by pitch, brightness, or loudness. Amusic participants showed some ability to extract contours in all three dimensions. For familiar melodies, amusic participants showed impairment in all conditions, perhaps reflecting the fact that the long-term memory representations of the familiar melodies were defined in pitch. In the contour discrimination task with novel melodies, amusic participants exhibited less impairment for loudness-based melodies than for pitch- or brightness-based melodies, suggesting some specificity of the deficit for spectral changes, if not for pitch alone. The results suggest pitch and brightness may not be processed by the same mechanisms as loudness, and that short-term memory for loudness contours may be spared to some degree in congenital amusia.

Pitch-Responsive Cortical Regions in Congenital Amusia.

Congenital amusia is a lifelong deficit in music perception thought to reflect an underlying impairment in the perception and memory of pitch. The neural basis of amusic impairments is actively debated. Some prior studies have suggested that amusia stems from impaired connectivity between auditory and frontal cortex. However, it remains possible that impairments in pitch coding within auditory cortex also contribute to the disorder, in part because prior studies have not measured responses from the cortical regions most implicated in pitch perception in normal individuals. We addressed this question by measuring fMRI responses in 11 subjects with amusia and 11 age- and education-matched controls to a stimulus contrast that reliably identifies pitch-responsive regions in normal individuals: harmonic tones versus frequency-matched noise. Our findings demonstrate that amusic individuals with a substantial pitch perception deficit exhibit clusters of pitch-responsive voxels that are comparable in extent, selectivity, and anatomical location to those of control participants. We discuss possible explanations for why amusics might be impaired at perceiving pitch relations despite exhibiting normal fMRI responses to pitch in their auditory cortex: (1) individual neurons within the pitch-responsive region might exhibit abnormal tuning or temporal coding not detectable with fMRI, (2) anatomical tracts that link pitch-responsive regions to other brain areas (e.g., frontal cortex) might be altered, and (3) cortical regions outside of pitch-responsive cortex might be abnormal. The ability to identify pitch-responsive regions in individual amusic subjects will make it possible to ask more precise questions about their role in amusia in future work.

Verbal and musical short-term memory: Variety of auditory disorders after stroke.

Auditory cognitive deficits after stroke may concern language and/or music processing, resulting in aphasia and/or amusia. The aim of the present study was to assess the potential deficits of auditory short-term memory for verbal and musical material after stroke and their underlying cerebral correlates with a Voxel-based Lesion Symptom Mapping approach (VLSM). Patients with an ischemic stroke in the right (N=10) or left (N=10) middle cerebral artery territory and matched control participants (N=14) were tested with a detailed neuropsychological assessment including global cognitive functions, music perception and language tasks. All participants then performed verbal and musical auditory short-term memory (STM) tasks that were implemented in the same way for both materials. Participants had to indicate whether series of four words or four tones presented in pairs, were the same or different. To detect domain-general STM deficits, they also had to perform a visual STM task. Behavioral results showed that patients had lower performance for the STM tasks in comparison with control participants, regardless of the material (words, tones, visual) and the lesion side. The individual patient data showed a double dissociation between some patients exhibiting verbal deficits without musical deficits or the reverse. Exploratory VLSM analyses suggested that dorsal pathways are involved in verbal (phonetic), musical (melodic), and visual STM, while the ventral auditory pathway is involved in musical STM.

Altered intrinsic connectivity of the auditory cortex in congenital amusia.

Congenital amusia, a neurodevelopmental disorder of music perception and production, has been associated with abnormal anatomical and functional connectivity in a right frontotemporal pathway. To investigate whether spontaneous connectivity in brain networks involving the auditory cortex is altered in the amusic brain, we ran a seed-based connectivity analysis, contrasting at-rest functional MRI data of amusic and matched control participants. Our results reveal reduced frontotemporal connectivity in amusia during resting state, as well as an overconnectivity between the auditory cortex and the default mode network (DMN). The findings suggest that the auditory cortex is intrinsically more engaged toward internal processes and less available to external stimuli in amusics compared with controls. Beyond amusia, our findings provide new evidence for the link between cognitive deficits in pathology and abnormalities in the connectivity between sensory areas and the DMN at rest.

Different neural networks are involved in audiovisual speech perception depending on the context.

How are we able to easily and accurately recognize speech sounds despite the lack of acoustic invariance? One proposed solution is the existence of a neural representation of speech syllable perception that transcends its sensory properties. In the present fMRI study, we used two different audiovisual speech contexts both intended to identify brain areas whose levels of activation would be conditioned by the speech percept independent from its sensory source information. We exploited McGurk audiovisual fusion to obtain short oddball sequences of syllables that were either (a) acoustically different but perceived as similar or (b) acoustically identical but perceived as different. We reasoned that, if there is a single network of brain areas representing abstract speech perception, this network would show a reduction of activity when presented with syllables that are acoustically different but perceived as similar and an increase in activity when presented with syllables that are acoustically similar but perceived as distinct. Consistent with the long-standing idea that speech production areas may be involved in speech perception, we found that frontal areas were part of the neural network that showed reduced activity for sequences of perceptually similar syllables. Another network was revealed, however, when focusing on areas that exhibited increased activity for perceptually different but acoustically identical syllables. This alternative network included auditory areas but no left frontal activations. In addition, our findings point to the importance of subcortical structures much less often considered when addressing issues pertaining to perceptual representations.

Visual change detection recruits auditory cortices in early deafness.

Although cross-modal recruitment of early sensory areas in deafness and blindness is well established, the constraints and limits of these plastic changes remain to be understood. In the case of human deafness, for instance, it is known that visual, tactile or visuo-tactile stimuli can elicit a response within the auditory cortices. Nonetheless, both the timing of these evoked responses and the functional contribution of cross-modally recruited areas remain to be ascertained. In the present study, we examined to what extent auditory cortices of deaf humans participate in high-order visual processes, such as visual change detection. By measuring visual ERPs, in particular the visual MisMatch Negativity (vMMN), and performing source localization, we show that individuals with early deafness (N=12) recruit the auditory cortices when a change in motion direction during shape deformation occurs in a continuous visual motion stream. Remarkably this "auditory" response for visual events emerged with the same timing as the visual MMN in hearing controls (N=12), between 150 and 300 ms after the visual change. Furthermore, the recruitment of auditory cortices for visual change detection in early deaf was paired with a reduction of response within the visual system, indicating a shift from visual to auditory cortices of part of the computational process. The present study suggests that the deafened auditory cortices participate at extracting and storing the visual information and at comparing on-line the upcoming visual events, thus indicating that cross-modally recruited auditory cortices can reach this level of computation.