Tone Sequences Research Articles

Functional reorganization of brain regions supporting artificial grammar learning across the first half year of life.

Pre-babbling infants can track nonadjacent dependencies (NADs) in the auditory domain. While this forms a crucial prerequisite for language acquisition, the neurodevelopmental origins of this ability remain unknown. We applied functional near-infrared spectroscopy in neonates and 6- to 7-month-old infants to investigate the neural substrate supporting NAD learning and detection using tone sequences in an artificial grammar learning paradigm. Detection of NADs was indicated by left prefrontal activation in neonates while by left supramarginal gyrus (SMG), superior temporal gyrus (STG), and inferior frontal gyrus activation in 6- to 7-month-olds. Functional connectivity analyses further indicated that the neonate activation pattern during the test phase benefited from a brain network consisting of prefrontal regions, left SMG and STG during the rest and learning phases. These findings suggest a left-hemispheric learning-related functional brain network may emerge at birth and serve as the foundation for the later engagement of these regions for NAD detection, thus, providing a neural basis for language acquisition.

Adaptation patterns and their associations with mismatch negativity: An electroencephalogram (EEG) study with controlled expectations.

Adaptation refers to the decreased neural response that occurs after repeated exposure to a stimulus. While many electroencephalogram (EEG) studies have investigated adaptation by using either single or multiple repetitions, the adaptation patterns under controlled expectations manifested in the two main auditory components, N1 and P2, are still largely unknown. Additionally, although multiple repetitions are commonly used in mismatch negativity (MMN) experiments, it is unclear how adaptation at different time windows contributes to this phenomenon. In this study, we conducted an EEG experiment with 37 healthy adults using a random stimulus arrangement and extended tone sequences to control expectations. We tracked the amplitudes of the N1 and P2 components across the first 10 tones to examine adaptation patterns. Our findings revealed an L-shaped adaptation pattern characterised by a significant decrease in N1 amplitude after the first repetition (N1 initial adaptation), followed by a continuous, linear increase in P2 amplitude after the first repetition (P2 subsequent adaptation), possibly indicating model adjustment. Regression analysis demonstrated that the peak amplitudes of both the N1 initial adaptation and the P2 subsequent adaptation significantly accounted for variance in MMN amplitude. These results suggest distinct adaptation patterns for multiple repetitions across different components and indicate that the MMN reflects a combination of two processes: the initial adaptation in the N1 and a continuous model adjustment effect in the P2. Understanding these processes separately could have implications for models of cognitive processing and clinical disorders.

Auditory distraction, time perception, and the role of age: ERP evidence from a large cohort study

Cognitive aging is typically associated with a higher susceptibility to distraction by concurrent, but task-irrelevant stimuli. Here, we studied the cognitive sub-processes involved in a sample of 484 healthy adults aged 20–70 years from the Dortmund Vital Study (Clinicaltrials.gov NCT05155397). Participants judged the duration of tone stimuli of a random sequence of long and short tones, having either a regular (standard) pitch or rare (deviant) pitch. Deviance-related ERPs were explored, reflecting neuro-cognitive correlates of pre-attentive deviance detection (MMN), attention allocation toward (P3a) and processing of (P3b) the deviance, and re-orienting toward the task-relevant stimulus feature (RON). Accuracy was reduced for deviant long tones, possibly due to withdrawing attention from processing the time information, making long stimuli appear shorter. This effect increased with age, and cluster-based permutation tests on the correlation of ERPs and age as well as linear mixed modeling indicated a decrease in MMN, an increase in P3a with long tones, and decreases in P3b and RON. This suggests a greater attentional orienting to the deviant stimulus feature and a reduced re-orienting to the task-relevant feature with increasing age.

Surprising sounds influence risky decision making

Adaptive behavior depends on appropriate responses to environmental uncertainty. Incidental sensory events might simply be distracting and increase errors, but alternatively can lead to stereotyped responses despite their irrelevance. To evaluate these possibilities, we test whether task-irrelevant sensory prediction errors influence risky decision making in humans across seven experiments (total n = 1600). Rare auditory sequences preceding option presentation systematically increase risk taking and decrease choice perseveration (i.e., increased tendency to switch away from previously chosen options). The risk-taking and perseveration effects are dissociable by manipulating auditory statistics: when rare sequences end on standard tones, including when rare sequences consist only of standard tones, participants are less likely to perseverate after rare sequences but not more likely to take risks. Computational modeling reveals that these effects cannot be explained by increased decision noise but can be explained by value-independent risky bias and perseveration parameters, decision biases previously linked to dopamine. Control experiments demonstrate that both surprise effects can be eliminated when tone sequences are presented in a balanced or fully predictable manner, and that surprise effects cannot be explained by erroneous beliefs. These findings suggest that incidental sounds may influence many of the decisions we make in daily life.

Rhythm Facilitates Auditory Working Memory via Beta-Band Encoding and Theta-Band Maintenance.

Rhythm, as a prominent characteristic of auditory experiences such as speech and music, is known to facilitate attention, yet its contribution to working memory (WM) remains unclear. Here, human participants temporarily retained a 12-tone sequence presented rhythmically or arrhythmically in WM and performed a pitch change-detection task. Behaviorally, while having comparable accuracy, rhythmic tone sequences showed a faster response time and lower response boundaries in decision-making. Electroencephalographic recordings revealed that rhythmic sequences elicited enhanced non-phase-locked beta-band (16 Hz-33 Hz) and theta-band (3 Hz-5 Hz) neural oscillations during sensory encoding and WM retention periods, respectively. Importantly, the two-stage neural signatures were correlated with each other and contributed to behavior. As beta-band and theta-band oscillations denote the engagement of motor systems and WM maintenance, respectively, our findings imply that rhythm facilitates auditory WM through intricate oscillation-based interactions between the motor and auditory systems that facilitate predictive attention to auditory sequences.

Physiological properties of auditory neurons responding to omission deviants in the anesthetized rat

SummaryThe detection of novel, low probability events in the environment is critical for survival. To perform this vital task, our brain is continuously building and updating a model of the outside world; an extensively studied phenomenon commonly referred to as predictive coding. Predictive coding posits that the brain is continuously extracting regularities from the environment to generate predictions. These predictions are then used to supress neuronal responses to redundant information, filtering those inputs, which then automatically enhances the remaining, unexpected inputs.We have recently described the ability of auditory neurons to generate predictions about expected sensory inputs by detecting their absence in an oddball paradigm using omitted tones as deviants. Here, we studied the responses of individual neurons to omitted tones by presenting individual sequences of repetitive pure tones, using both random and periodic omissions, presented at both fast and slow rates in the inferior colliculus and auditory cortex neurons of anesthetized rats. Our goal was to determine whether feature-specific dependence of these predictions exists. Results showed that omitted tones could be detected at both high (8 Hz) and slow repetition rates (2 Hz), with detection being more robust at the non-lemniscal auditory pathway.

Time scale of adaptation at the tonal sequence processing in the awake mice auditory cortex neurons

The study was firstly carried out on stimulus-specific adaptation of neurons in the primary and anterior fields of the awake house mice auditory cortex to sound sequences of four 100-ms tonal signals, with frequency of tones corresponding to the neuronal characteristic frequency, and also with the inter-tone interval constant for one sequence and varying from 0 to 2000 ms in different sequences. The analysis of the data obtained showed the adaptation effect in the responses of all studied primary auditory cortex neurons, which was observed as the absence or significant decrease in activity evoked by the components of a series of tones following the 1st, at inter-stimulus intervals of 0–500 ms. A quantitative assessment of the adaptation effects as a function of inter-stimulus intervals within the tonal sequence, performed over whole population of studied neurons, showed that the individual time scales of adaptation of neurons varied significantly, which may be crucial for the formation of optimal time windows for the processing of grouping and separation of sound events, which are important both for perception of animal vocalizations and human speech.

Cortical-subcortical interactions underlie processing of auditory predictions measured with 7T fMRI.

Perception integrates both sensory inputs and internal models of the environment. In the auditory domain, predictions play a critical role because of the temporal nature of sounds. However, the precise contribution of cortical and subcortical structures in these processes and their interaction remain unclear. It is also unclear whether these brain interactions are specific to abstract rules or if they also underlie the predictive coding of local features. We used high-field 7T functional magnetic resonance imaging to investigate interactions between cortical and subcortical areas during auditory predictive processing. Volunteers listened to tone sequences in an oddball paradigm where the predictability of the deviant was manipulated. Perturbations in periodicity were also introduced to test the specificity of the response. Results indicate that both cortical and subcortical auditory structures encode high-order predictive dynamics, with the effect of predictability being strongest in the auditory cortex. These predictive dynamics were best explained by modeling a top-down information flow, in contrast to unpredicted responses. No error signals were observed to deviations of periodicity, suggesting that these responses are specific to abstract rule violations. Our results support the idea that the high-order predictive dynamics observed in subcortical areas propagate from the auditory cortex.

Deficits in congenital amusia: Pitch, music, speech, and beyond

Congenital amusia is a neurodevelopmental disorder characterized by deficits of music perception and production, which are related to altered pitch processing. The present study used a wide variety of tasks to test potential patterns of processing impairment in individuals with congenital amusia (N = 18) in comparison to matched controls (N = 19), notably classical pitch processing tests (i.e., pitch change detection, pitch direction of change identification, and pitch short-term memory tasks) together with tasks assessing other aspects of pitch-related auditory cognition, such as emotion recognition in speech, sound segregation in tone sequences, and speech-in-noise perception. Additional behavioral measures were also collected, including text reading/copying tests, visual control tasks, and a subjective assessment of hearing abilities. As expected, amusics' performance was impaired for the three pitch-specific tasks compared to controls. This deficit of pitch perception had a self-perceived impact on amusics’ quality of hearing. Moreover, participants with amusia were impaired in emotion recognition in vowels compared to controls, but no group difference was observed for emotion recognition in sentences, replicating previous data. Despite pitch processing deficits, participants with amusia did not differ from controls in sound segregation and speech-in-noise perception. Text reading and visual control tests did not reveal any impairments in participants with amusia compared to controls. However, the copying test revealed more numerous eye-movements and a smaller memory span. These results allow us to refine the pattern of pitch processing and memory deficits in congenital amusia, thus contributing further to understand pitch-related auditory cognition. Together with previous reports suggesting a comorbidity between congenital amusia and dyslexia, the findings call for further investigation of language-related abilities in this disorder even in the absence of neurodevelopmental language disorder diagnosis.

Influence of degree of learning on rate of forgetting of tonal sequences.

Initial performance is frequently equated in studies that compare forgetting rates across groups. However, since the encoding capacity of different groups can be different, some procedures to match initial degree of learning need to be implemented, adding confounding variables such as longer exposures to the material, which would create memories of a different age. Slamecka and McElree Journal of Experimental Psychology: Learning, Memory, and Cognition,9, 384-397, (1983) and our previous work found that the rate of forgetting was independent from initial degree of learning using verbal material. The present study seeks to determine whether this pattern holds true when undertaken with nonverbal material. In two experiments, we manipulate initial degree of learning by varying the number of presentations of the material and studying the effect on the forgetting rates. A set of 30 tonal sequences were presented to young, healthy participants either once or three times. Forgetting was evaluated in a yes/no recognition paradigm immediately and 1 hour or 24 hours after the study phase. A different subset of 10 sequences was tested along with 10 nontargets at each retention interval. The results of these experiments showed that initial acquisition was modulated by the number of repetitions. However, the forgetting rates were independent of initial degree of learning. These results are in keeping with the pattern found by Slamecka and McElree, and in our own previous studies. They suggest that the pattern of parallel forgetting after different levels of initial learning is not limited to verbal material.

Theta oscillations linked to auditory informativeness and context disambiguation.

Accurate predictions and the processing of prediction error signals can be important for efficient interaction with the auditory environment. In a reanalysis of data from Simal et al. (2021), who found that informative tones elicited increased N1 and P2 event-related potential components, we sought to identify electrophysiological indicators in the time-frequency domain associated with disambiguation of the hearing context and prediction of forthcoming stimulation. Participants heard two isochronous sequences of pure tones separated by a silent retention interval. A sequence could contain one, three, or five tones. Fifteen participants heard the three load conditions randomly intermixed. In this case, when sequence length was unknown, the second and fourth tone during encoding contained information allowing the prediction of another tone. Other participants heard the sequences blocked by sequence length, and the second and fourth tone of the sequences provided no new information (and hence were not informative). We used wavelet analysis and Hilbert transform methods to analyse the oscillatory activity related to tone informativeness. We found a significant increase in theta (4-7 Hz) amplitude following a tone that was informative and allowed prediction, in comparison with a tone that carried no predictive information. Previous work suggests increased theta amplitude is linked with task switching and an increase in cognitive control. We suggest informative tones recruit higher-level control processes involved in prediction of upcoming auditory events.

Musical Advantage in Lexical Tone Perception Hinges on Musical Instrument

Different musical instruments have different pitch processing demands. However, correlational studies have seldom considered the role of musical instruments in music-to-language transfer. Addressing this research gap could contribute to a nuanced understanding of music-to-language transfer. To this end, we investigated whether pitched musicians had a unique musical advantage in lexical tone perception relative to unpitched musicians and nonmusicians. Specifically, we compared Cantonese pitched musicians, unpitched musicians, and nonmusicians on Thai tone discrimination and sequence recall. In the Thai tone discrimination task, the pitched musicians outperformed the unpitched musicians and the nonmusicians. Moreover, the unpitched musicians and the nonmusicians performed similarly. In the Thai tone sequence recall task, both pitched and unpitched musicians recalled level tone sequences more accurately than the nonmusicians, but the pitched musicians showed the largest musical advantage. However, the three groups recalled contour tone sequences with similar accuracy. Collectively, the pitched musicians had a unique musical advantage in lexical tone discrimination and the largest musical advantage in level tone sequence recall. From a theoretical perspective, this study offers correlational evidence for the Precision element of the OPERA hypothesis. The choice of musical instrumental may matter for music-to-language transfer in lexical tone discrimination and level tone sequence recall.

Aberrant Cardiac Interoception in Psychosis.

There is mounting evidence that cardiac interoception, the perception of one's heartbeat, is central to affective experiences. It has been proposed that symptoms of psychosis could arise from interoceptive dysfunction. Here we hypothesized that people with psychotic disorders would have a specific impairment in cardiac interoception, over and above broader perceptual deficits. 43 adults with a history of psychosis (31 schizophrenia, 12 schizoaffective disorder) and 41 matched control participants completed a heart rate discrimination task. Participants responded to whether they perceived a sequence of auditory tones to be faster or slower than their heart rate. By trialing a range of auditory tone rates, we estimated a threshold for each participant, the difference between perceived heart rate and actual heart rate. To test whether differences were specific to interoception, participants completed an exteroceptive control condition, testing their discrimination of the rate of 2 sets of audible sounds instead of heart rate. Participants with a history of psychosis had greater absolute differences between perceived and actual heart rate, indicating over- or under-estimation of heart rate compared to healthy controls. This difference was specific to the interoceptive condition, and not explained by group differences in exteroceptive perception. Psychotic disorders are associated with misestimation of heart rate. Further research may elucidate whether interoceptive abnormalities contribute to specific symptoms such as somatic delusions or affective features, and whether interoception could be a treatment target in psychotic disorders.

An auditory brain-computer interface based on selective attention to multiple tone streams.

In this study, we attempted to improve brain-computer interface (BCI) systems by means of auditory stream segregation in which alternately presented tones are perceived as sequences of various different tones (streams). A 3-class BCI using three tone sequences, which were perceived as three different tone streams, was investigated and evaluated. Each presented musical tone was generated by a software synthesizer. Eleven subjects took part in the experiment. Stimuli were presented to each user's right ear. Subjects were requested to attend to one of three streams and to count the number of target stimuli in the attended stream. In addition, 64-channel electroencephalogram (EEG) and two-channel electrooculogram (EOG) signals were recorded from participants with a sampling frequency of 1000 Hz. The measured EEG data were classified based on Riemannian geometry to detect the object of the subject's selective attention. P300 activity was elicited by the target stimuli in the segregated tone streams. In five out of eleven subjects, P300 activity was elicited only by the target stimuli included in the attended stream. In a 10-fold cross validation test, a classification accuracy over 80% for five subjects and over 75% for nine subjects was achieved. For subjects whose accuracy was lower than 75%, either the P300 was also elicited for nonattended streams or the amplitude of P300 was small. It was concluded that the number of selected BCI systems based on auditory stream segregation can be increased to three classes, and these classes can be detected by a single ear without the aid of any visual modality.

Carrier-frequency specific omission-related neural activity in ordered sound sequences is independent of omission-predictability.

Regularities in our surroundings lead to predictions about upcoming events. Previous research has shown that omitted sounds during otherwise regular tone sequences elicit frequency-specific neural activity related to the upcoming but omitted tone. We tested whether this neural response is depending on the unpredictability of the omission. Therefore, we recorded magnetencephalography (MEG) data while participants listened to ordered or random tone sequences with omissions occurring either ordered or randomly. Using multivariate pattern analysis shows that the frequency-specific neural pattern during omission within ordered tone sequences occurs independent of the regularity of the omissions. These results suggest that the auditory predictions based on sensory experiences are not immediately updated by violations of those expectations.

Attention-Modulated Cortical Responses as a Biomarker for Tinnitus.

Attention plays an important role in not only the awareness and perception of tinnitus but also its interactions with external sounds. Recent evidence suggests that attention is heightened in the tinnitus brain, likely as a result of relatively local cortical changes specific to deafferentation sites or global changes that help maintain normal cognitive capabilities in individuals with hearing loss. However, most electrophysiological studies have used passive listening paradigms to probe the tinnitus brain and produced mixed results in terms of finding a distinctive biomarker for tinnitus. Here, we designed a selective attention task, in which human adults attended to one of two interleaved tonal (500 Hz and 5 kHz) sequences. In total, 16 tinnitus (5 females) and 13 age- and hearing-matched control (8 females) subjects participated in the study, with the tinnitus subjects matching the tinnitus pitch to 5.4 kHz (range = 1.9-10.8 kHz). Cortical responses were recorded in both passive and attentive listening conditions, producing no differences in P1, N1, and P2 between the tinnitus and control subjects under any conditions. However, a different pattern of results emerged when the difference was examined between the attended and unattended responses. This attention-modulated cortical response was significantly greater in the tinnitus than control subjects: 3.9-times greater for N1 at 5 kHz (95% CI: 2.9 to 5.0, p = 0.007, ηp2 = 0.24) and 3.0 for P2 at 500 Hz (95% CI: 1.9 to 4.5, p = 0.026, ηp2 = 0.17). We interpreted the greater N1 modulation as local neural changes specific to the tinnitus frequency and the greater P2 as global changes to hearing loss. These two cortical measures were used to differentiate between the tinnitus and control subjects, producing 83.3% sensitivity and 76.9% specificity (AUC = 0.81, p = 0.006). These results suggest that the tinnitus brain is more plastic than that of the matched non-tinnitus controls and that the attention-modulated cortical response can be developed as a clinically meaningful biomarker for tinnitus.

Individual differences in auditory perception predict learning of non-adjacent tone sequences in 3-year-olds.

Auditory processing of speech and non-speech stimuli oftentimes involves the analysis and acquisition of non-adjacent sound patterns. Previous studies using speech material have demonstrated (i) children's early emerging ability to extract non-adjacent dependencies (NADs) and (ii) a relation between basic auditory perception and this ability. Yet, it is currently unclear whether children show similar sensitivities and similar perceptual influences for NADs in the non-linguistic domain. We conducted an event-related potential study with 3-year-old children using a sine-tone-based oddball task, which simultaneously tested for NAD learning and auditory perception by means of varying sound intensity. Standard stimuli were A × B sine-tone sequences, in which specific A elements predicted specific B elements after variable × elements. NAD deviants violated the dependency between A and B and intensity deviants were reduced in amplitude. Both elicited similar frontally distributed positivities, suggesting successful deviant detection. Crucially, there was a predictive relationship between the amplitude of the sound intensity discrimination effect and the amplitude of the NAD learning effect. These results are taken as evidence that NAD learning in the non-linguistic domain is functional in 3-year-olds and that basic auditory processes are related to the learning of higher-order auditory regularities also outside the linguistic domain.

Sandhi-based predictability of pitch accent facilitates word recognition in Kansai Japanese speakers.

This study investigates the predictability effects of pitch accent on word recognition using the sandhi rule in Kansai Japanese (KJ). Native KJ speakers and native Tokyo Japanese (TJ) speakers (control group) saw images of four objects while hearing modifier + noun phrases and selected the corresponding image as quickly as possible. The word-initial tone of the noun's initial mora was predictable or unpredictable based on the tone of the preceding modifier's final mora in KJ but not in TJ. Experiment 1 found faster reaction times in the predictable conditions compared with the unpredictable conditions in KJ speakers but only when the modifier had an all-low tone sequence. This finding suggests that a modifier-ending that changes following the sandhi rule can function as a reliable cue to constrain an upcoming tone, whereas a modifier-ending tone that remains the same as in the citation form cannot (although the next tone is predictable). Unexpectedly, we found the same effect, albeit weaker, in TJ speakers. Experiment 2 replicated this effect and additionally showed that the facilitation effect was not due to TJ speakers having sufficient exposure to KJ to be familiar with the KJ sandhi rule. We speculate that the effect in TJ speakers is related to a language universal constraint against a sequence of low tones without a high tone within a phonological word, which may urge listeners to listen for a high tone in the upcoming input.

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.

Long-Horizon Associative Learning Explains Human Sensitivity to Statistical and Network Structures in Auditory Sequences.

Networks are a useful mathematical tool for capturing the complexity of the world. In a previous behavioral study, we showed that human adults were sensitive to the high-level network structure underlying auditory sequences, even when presented with incomplete information. Their performance was best explained by a mathematical model compatible with associative learning principles, based on the integration of the transition probabilities between adjacent and nonadjacent elements with a memory decay. In the present study, we explored the neural correlates of this hypothesis via magnetoencephalography (MEG). Participants (N = 23, 16 females) passively listened to sequences of tones organized in a sparse community network structure comprising two communities. An early difference (∼150 ms) was observed in the brain responses to tone transitions with similar transition probability but occurring either within or between communities. This result implies a rapid and automatic encoding of the sequence structure. Using time-resolved decoding, we estimated the duration and overlap of the representation of each tone. The decoding performance exhibited exponential decay, resulting in a significant overlap between the representations of successive tones. Based on this extended decay profile, we estimated a long-horizon associative learning novelty index for each transition and found a correlation of this measure with the MEG signal. Overall, our study sheds light on the neural mechanisms underlying human sensitivity to network structures and highlights the potential role of Hebbian-like mechanisms in supporting learning at various temporal scales.