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Griffiths, T. D.

Publications and source records attributed to Griffiths, T. D..

At least 19 recordsLinked to original sources

Ordinal position in auditory sequences is encoded in population dynamics in macaque frontal cortex

The ability to extract structure from sensory sequences requires tracking not only stimulus identity but also ordinal position within a sequence. How and where ordinal information is represented in the primate brain remains unclear. Here, we recorded activity in populations of single neurons simultaneously from auditory cortex and ventrolateral prefrontal cortex in macaques passively listening to structured auditory sequences. Population-level analyses revealed that frontal cortex activity evolved progressively across the sequence, occupying distinct regions of neural state space for successive ordinal positions. In contrast, auditory cortex population activity reset with each element, producing stereotyped, stimulus-locked trajectories. Consistent with this dissociation, frontal cortex populations robustly decoded ordinal position independently of stimulus identity, whereas auditory cortex showed weak positional decoding despite strong identity representations. Frontal neurons further exhibited longer intrinsic timescales and reduced synchronization to element presentation, supporting integration of information across multiple elements. Together, these findings identify frontal activity as a key substrate for ordinal position encoding during auditory sequence processing, while auditory cortex primarily supports element-specific sensory representations.

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Sensing the heart, seeing the world: Neural mechanisms of attentional allocation between interoception and exteroception

Adaptive behaviour requires the flexible allocation of attention between sensory information arising from the external environment (exteroception) and signals originating within the body (interoception). While the neural mechanisms supporting exteroceptive attention have been extensively characterised, considerably less is known about how attention is allocated between competing interoceptive and exteroceptive sources of information. To address this question, we used functional magnetic resonance imaging (fMRI) to compare cardiac interoceptive attention during heartbeat counting with a carefully matched visual target counting task. Importantly, external visual input was held constant during both tasks, and behavioural accuracy and subjective confidence ratings for task difficulty did not differ significantly between conditions. This provided a controlled comparison in which attention was selectively allocated between internal bodily signals and external sensory information. Cardiac interoceptive and visual exteroceptive attention engaged largely distinct cortical networks. Cardiac interoceptive attention recruited a distributed insula-centred network supporting interoceptive processing and cognitive control. In contrast, visual target counting engaged a dorsal frontoparietal attention network and selectively shaped activity within visual cortex, enhancing regions representing task-relevant central visual information while suppressing regions representing task-irrelevant peripheral visual information. Despite this functional segregation, activity within these systems was not independent of where attention was directed. Exteroceptive attention suppressed activity within the posterior insula, suggesting down-regulation of interoceptive processing. Conversely, peripheral visual regions remained suppressed during interoceptive attention, suggesting that externally directed sensory processing is also down-regulated when attention is directed towards the body. More accurate heartbeat counting was additionally associated with less engagement of the right inferior parietal lobule, consistent with reduced bottom-up attentional capture by external sensory information. Together, these findings are consistent with competitive allocation of attentional resources between neural systems supporting internal bodily signals and external sensory information. More broadly, they provide a system-level account of how the human brain flexibly balances internal and external information during goal-directed behaviour.

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Auditory Working Memory and Sound Segregation Ability Predict Speech-in-Noise in Adult Cochlear Implant Users

ObjectivesOutcomes following cochlear implantation vary substantially across adult recipients, and the cognitive and perceptual factors contributing to this variability are not fully understood. This poses a challenge for developing strategies to improve cochlear implant outcomes, as such approaches require a clearer understanding of the mechanisms underlying individual listening difficulties. In this study, we investigated auditory cognitive measures in cochlear implant (CI) users to further elucidate the origins of this variability. DesignThirty-seven adult cochlear implant users completed measures of auditory cognition, comprising auditory working memory (AWM) and sound segregation ability, measured using an auditory figure-ground task (AFG), as well as measures of peripheral temporal and spectral processing, comprising the temporal modulation detection threshold (TMDT) and spectral ripple discrimination threshold (SRDT). Speech perception outcomes were assessed using word-in-noise (WIN) and sentence-in-noise (SIN) tasks. Separate multiple linear regression models evaluated the unique contribution of the auditory cognition measures to WIN and SIN performance, after accounting for the peripheral measures. ResultsBoth regression models explained a substantial proportion of variance in speech-in-noise outcomes (WIN: adjusted R{superscript 2} = 0.55; SIN: adjusted R{superscript 2}=0.57, both p < 0.001). For WIN performance, AFG and AWM were significant predictors. A similar pattern was found for SIN performance, where lower AWM ability and poorer AFG segregation were linked to poorer sentence listening in noise. No significant effects of spectral ripple discrimination or temporal modulation detection were observed in either model, even though both were significantly correlated with WIN performance. ConclusionsThese findings indicate that auditory working memory and sound segregation ability are robust predictors of speech-in-noise outcomes in adult cochlear implant users, across both word- and sentence-level measures. Together, the results may help explain why speech-in-noise outcomes remain highly variable among CI users, even when basic sensory encoding abilities are taken into account. Incorporating measures of auditory working memory and fundamental sound segregation may therefore improve outcome prediction and help in developing more individualised rehabilitation strategies.

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Auditory Working Memory Mediates the Relationship between Musical Sophistication and Speech-in-noise Perception

Understanding speech in noisy environments (SPIN) is an important everyday ability, and engaging in musical activities has been proposed as a factor that may support this ability. However, the cognitive mechanisms underlying a potential musical advantage in SPIN perception remain unclear. Here we investigated whether musical sophistication is associated with better SPIN perception in a large population-based sample, and whether this relationship is mediated by auditory working memory (AWM), verbal working memory (VWM), or non-verbal intelligence. We recruited 203 participants and measured SPIN perception at both word and sentence levels. Musical sophistication was assessed using the Goldsmiths Musical Sophistication Index (Gold-MSI). AWM was measured using delayed matching of tone frequency or the modulation rate of amplitude modulated white noise, VWM was based on backward digit span task, and non-verbal intelligence used matrix reasoning. Mediation analyses revealed that AWM fully mediated the relationship between musical sophistication and SPIN perception, whereas VWM showed no mediation effect. Non-verbal intelligence showed a partial mediating effect. Additional control analyses using structural equation modelling revealed that the indirect effect through AWM remained significant after accounting for age, hearing thresholds, and non-verbal intelligence. Together, these findings suggest that individuals with greater musical sophistication demonstrate better daily life listening abilities, and that superior auditory working memory may be the key cognitive mechanism underlying this advantage.

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Prior expectation shapes the emotional response to sounds: behavioural and neural correlates

Prior expectations are known to shape perception especially when a stimulus is ambiguous. Bayesian models of cognition posit perception is a precision-weighted combination of top-down and bottom-up information. We consider here affective responses to highly salient stimuli for which a dominant role of bottom-up processing has previously been emphasised. We study how predictions alter the perception of emotional stimuli in a paradigm in which neutral and aversive sounds were preceded by either predictive or non-predictive cues. Cues predicted the type of sound with 100% or 50% probability. Behavioural measures of trial-by-trial expectation and perceived aversiveness were collected before and after stimulus presentation, respectively. We show that prior expectations biased the perceived aversiveness of sounds towards predictions, but only when subjective expectations were considered (as opposed to the objective expectation based on conditional probability). Neural responses were recorded using EEG. During sound processing, we found P3 and LPP components were increased after non-predictive cues, but only for affective stimuli. Time-Frequency results uncovered a role of alpha-beta oscillations in the precision of predictions, as well as in the processing of unexpected stimuli. Our results indicate expectations directly alter the perception of affective stimuli and its processing, and emphasise the importance of behavioural measures to characterize this relationship.

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Heterogeneity in neural network engagement supports individual differences in top-down attention

Top-down attention enables selective prioritisation of goal-relevant information, yet how attentional control varies across individuals remains unclear, particularly in relation to sensory processing. Here, we combined magnetoencephalography (MEG) and pupillometry--in older adults performing a spatial cueing task--to examine both shared and subject-specific aspects of top-down attention. Informative spatial cues elicited sustained activity in fronto-parietal and sensory regions, alpha lateralisation, and increased pupil dilation, replicating established neural and physiological markers. Crucially, these group-level patterns were accompanied by systematic intersubject variability: individuals with greater hearing loss showed increased preparatory engagement of precentral and postcentral gyri, and variation in pupil dilation predicted activity in frontal regions. These results reveal that top-down attention arises from heterogeneous network configurations shaped by sensory processing and strategic resource allocation. Overall, our findings underscore the need to move beyond group averages to capture the neural architecture underlying individual differences in top-down attention.

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Brain-wide single-neuron bases of working memory for sounds in humans

In order to understand the constantly changing acoustic world our brains must maintain elements of auditory scenes in memory. The neural mechanisms for this fundamental process remain unclear. Here, we report human intracranial recordings of 1269 single neurons while participants performed a non-verbal auditory working memory task that required adjustment of a tone frequency to match a target. We found neurons within hippocampus, insula and cingulate cortex, for which firing rates were modulated at different phases of the task, particularly during maintenance and adjustment. For the majority of the neurons modulated during maintenance there was a striking suppression of activity rather than increased activity. Across the entire neuronal population, state-space analysis demonstrated attractor-like states corresponding to different task phases. Behaviorally, more neurons were modulated at the beginning of the maintenance phase in trials when participants performed better. State-space analysis was consistent with greater attractor-like activity during the adjustment phase supporting better performance. These data support the existence of a widely distributed neural code for auditory working memory that determines related behavior based on attractor-like states.

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Auditory-cognitive determinants of speech-in-noise perception: structural equation modelling of a large sample

Problems understanding speech-in-noise (SIN) are commonly associated with peripheral hearing loss. But pure tone audiometry (PTA) alone fails to fully explain SIN ability. This is because SIN perception is based on complex interactions between peripheral hearing, central auditory processing (CAP) and other cognitive abilities. We assessed interaction between these factors and age using a multivariate approach that allows the modelling of directional effects on theoretical constructs: structural equation modelling. We created a model to explain SIN using latent constructs for sound segregation, auditory (working) memory, and SIN perception, as well as PTA, age and measures of non-verbal reasoning. In a sample of 207 participants aged 18-81 years old, age was the biggest determinant of SIN ability, followed by auditory memory. PTA did not contribute to SIN directly, although it modified sound segregation ability, which covaried with auditory memory. A second model, using a CAP latent structure formed by measures of sound segregation, auditory memory, and temporal processing, revealed CAP to be the largest determinant of SIN ahead of age. Furthermore, we demonstrated the impact of PTA and non-verbal reasoning on SIN are mediated by their influence on CAP. Our results highlight the importance of central auditory processing in speech-in-noise perception.

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The role of attention in the generation of anticipatory potentials to affective stimuli: an ERP and source analysis study

Anticipatory EEG signals are characterised by the occurrence of negative slow cortical potentials. This negativity is posed to be enhanced when expecting highly emotional stimuli; however, the specific role attention plays in its generation is unclear, as emotional content is more salient and arousing, and thus recruits higher attentional resources. Here, affective anticipation signals were recorded in 35 participants with EEG, and their brain sources elucidated using multiple sparse priors algorithm. Using a cued-paradigm, the category of a sound being negatively valenced or neutral could be predicted with a 68% accuracy. To shift attentional resources away from the emotional content, participants were instructed to listen and respond to a burst of white noise that occurred on 9% of trials. Results showed slower reaction times following the aversive cue, yet no difference in EEG amplitude between aversive and neutral anticipation. Response times positively correlated with EEG amplitude - participants with stronger negativity were faster to respond. EEG source reconstruction demonstrated no differences between conditions, and showed activation of areas within the salience network including insula, somatosensory cortex, and thalamus. The current results suggest that anticipatory EEG negativity is an index of attentional resource-allocation during the anticipation period and does not reflect the emotional content of upcoming stimuli.

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Neural entrainment to pitch changes of auditory targets in noise

Neural entrainment to certain acoustic features can predict speech-in-noise perception, but these features are difficult to separate. We measured neural responses to both natural speech-in-noise and stimuli (auditory figure-ground) that simulate speech-in-noise without any acoustic or linguistic confound such as stress contour and semantics. The figure-ground stimulus is formed by multiple temporally coherent pure-tone components embedded in a random tone cloud. Previous work has shown that discrimination of dynamic figure-ground based on the fundamental frequency (F0) of natural speech predicts speech-in-noise recognition independent of hearing and age. In this study, we compared the brain substrate for the figure-ground analysis based on the F0 contour and a statistically similar 1/f contour with speech-in-noise. We used the temporal response function to predict the electroencephalography responses to the frequency trajectories of the auditory targets. We demonstrate that the brain significantly tracked the pitch changes in both AFG conditions (F0 and 1/F tracking) and a sentence-in-noise condition (F0 tracking) at similar latencies, but at similar magnitudes only when tracking the F0 contour. The pitch-tracking accuracy was consistently high across the delta and theta bands for the AFG condition but not for speech. Sensor-space analysis revealed that speech-in-noise performance correlated with the positive peak amplitude of the F0 figure-ground at 100 ms. Source-space analysis revealed bilateral temporal lobe and hippocampal generators, and strong tracking in the superior parietal lobe for auditory figures and natural speech. In conclusion, our findings demonstrate that the human brain reliably tracks the F0 trajectory of both speech and a non-linguistic figure in noise, with speech tracking showing reduced accuracy in the theta band compared to figure-ground tracking. Despite the difference in prediction accuracy, we reveal striking similarities in neural entrainment patterns and source locations between the two paradigms. These results suggest that neural entrainment engages high-level cortical mechanisms independent of linguistic content. Furthermore, we show that TRF peak amplitude serves as a potential biomarker for speech-in-noise ability, highlighting possible clinical applications.

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British Version of the Iowa Test of Consonant Perception

The Iowa Test of Consonant Perception (ITCP) is a single-word closed-set speech- in-noise test with well-balanced phonetic features that provides a reliable testing option for real-world listening. Objectives. The current study aimed to establish a UK version of the test (B-ITCP) based on the British received pronunciation. Design. We conducted a validity test with 46 participants using the B-ITCP test, a sentence-in- noise test, and audiogram. Results. The B-ITCP demonstrated excellent test-retest reliability, cross-talker validity, and good convergent validity, consistent with the US results. Conclusions. These findings suggest that B-ITCP is a reliable measure of speech-in-noise perception, to facilitate comparative or combined studies in USA and UK. All materials (application and scripts) to run or construct the B-ITCP and ITCP are freely available online.

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Spatial selective auditory attention is preserved in older age but is degraded by peripheral hearing loss

Interest in how ageing affects attention is long-standing, although interactions between sensory and attentional processing in older age have not been systematically studied. Here, we examined interactions between peripheral hearing and selective attention in a spatialised cocktail party listening paradigm, in which three talkers spoke different sentences simultaneously and participants were asked to report the sentence spoken by a talker at a particular location. By comparing a sample of older (N = 61; age = 55- 80 years) and younger (N = 58; age = 18-35 years) adults, we show that, as a group, older adults benefit as much as younger adults from preparatory spatial attention. Although, for older adults, this benefit significantly reduces with greater age-related hearing loss. These results demonstrate that older adults without hearing loss retain the ability to direct spatial selective attention, but this ability deteriorates with age-related hearing loss. Thus, reductions in spatial selective attention likely contribute to difficulties communicating in social settings for older adults with age-related hearing loss. Overall, these findings demonstrate a relationship between mild perceptual decline and attention in older age.

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Immediate neural network impact after the loss of a semantic hub

The human brain extracts meaning from the world using an extensive neural system for semantic knowledge. Whether such broadly distributed systems1-3 crucially depend on or can compensate for the loss of one of their highly interconnected hubs4-6 is controversial4. The strongest level of causal evidence for the role of a brain hub is to evaluate its acute network-level impact following disconnection and any rapid functional compensation that ensues. We report rare neurophysiological data from two patients who underwent awake intracranial recordings during a speech prediction task immediately before and after neurosurgical treatment that required disconnection of the left anterior temporal lobe (ATL), a crucial hub for semantic knowledge4-6. Informed by a predictive coding framework, we tested three sets of hypotheses including diaschisis causing disruption in interconnected sites7 and incomplete or complete compensation by other language-critical and speech processing sites8-10. Immediately after ATL disconnection, we observed highly specific neurophysiological alterations in the recorded fronto-temporal network, including abnormally magnified high gamma responses to the speech sounds in auditory cortex. We also observed evidence for rapid compensation, seen as focal increases in effective connectivity involving language-critical sites in the inferior frontal gyrus and speech processing sites in auditory cortex. However, compensation was incomplete, in part because after ATL disconnection speech prediction signals were depleted in auditory cortex. This study provides direct causal evidence for a semantic hub in the human brain and shows striking neural impact and a rapid attempt at compensation in a neural network after the loss of one of its hubs.

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EEG Responses to Auditory Figure-Ground Perception

Speech-in-noise difficulty is commonly reported among hearing-impaired individuals. Recent work has established generic behavioural measures of sound segregation and grouping that are related to speech-in-noise processing but do not require language. In this study, we assessed potential clinical electroencephalographic (EEG) measures of central auditory grouping (stochastic figure-ground test) and speech-in-noise perception (speech-in-babble test) with and without relevant tasks. Auditory targets were presented within background noise (16 talker-babble or randomly generated pure-tones) in 50% of the trials and composed either a figure (pure-tone frequency chords repeating over time) or speech (English names). EEG was recorded while participants were presented with the target stimuli (figure or speech) under different attentional states (relevant task or visual-distractor task). EEG time-domain analysis demonstrated enhanced negative responses during detection of both types of auditory targets within the time window 650-850 ms but only figure detection produced significantly enhanced responses under the distracted condition. Further single-channel analysis showed that simple vertex-to-mastoid acquisition defines a very similar response to more complex arrays based on multiple channels. Evoked-potentials to the generic figure-ground task therefore represent a potential clinical measure of grouping relevant to real-world listening that can be assessed irrespective of language knowledge and expertise even without a relevant task.

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Distribution of multi-unit pitch responses recorded intracranially from human auditory cortex

The perception of pitch requires the abstraction of stimulus properties related to the spectrotemporal structure of sound. Previous studies utilizing both animal electrophysiology and human imaging have indicated the presence of a center for pitch representation in the auditory cortex. Recent data from our own group - examining local field potentials (LFPs) in humans - indicate more widely distributed pitch-associated responses within the auditory cortex (Gander et al., 2019). To probe this with greater spatial resolution, we examined multi-unit activity related to three different auditory stimuli, in seven epilepsy patients who were implanted with high-impedance electrodes in auditory cortex for the clinical purpose of localizing seizures. The stimuli were regular-interval noise (RIN) with a pitch strength that is related to the temporal regularity, and pitch value determined by repetition rate, and harmonic complexes with missing fundamentals. We demonstrated increases in spiking activity in 69 of 104 (66%) responsive multiunit activity in auditory cortex due to pitch-associated stimuli. Importantly, these responses were distributed across the entire extent of Heschls gyrus (HG), in both primary and non-primary areas, rather than isolated to a specific region, and this finding was evident regardless of the stimulus presented. These findings are the first multi-unit pitch responses recorded from humans, and align with a recent study in macaques (Kikuchi et al., 2019) demonstrating that both local field potential and unit responses to pitch-inducing stimuli are distributed throughout auditory cortex. Significance StatementThe perception of pitch is a fundamental acoustic attribute that is mediated by the auditory system. Despite its importance, there is still debate as to the precise areas responsible for its encoding, which may be due to differences in the recording measures and choices of stimuli used in previous studies. Here, we present the first study to measure multi-unit pitch responses in the auditory cortices of intracranially-implanted humans. Importantly, we demonstrate reliable responses to three different pitch-inducing paradigms that are distributed throughout Heschls gyrus, rather than being localized to a particular region. These data provide a bridge across animal and human studies, and aid in our understanding of the processing of a critical attribute of acoustic stimuli.

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Neural correlates of individual differences in speech-in-noise performance in a large cohort of cochlear implant users

ObjectivesUnderstanding speech in noise (SiN) is a complex task that recruits multiple cortical subsystems. Individuals vary in their ability to understand SiN. This cannot be explained by simple peripheral hearing profiles, but recent work by our group (Kim et al., 2021, Neuroimage) highlighted central neural factors underlying the variance in SiN ability in normal hearing (NH) subjects. The current study examined neural predictors of speech-in-noise ability in a large cohort of cochlear-implant (CI) users, with the long-term goal of developing a simple electrophysiological correlate that could be implemented in clinics. DesignWe recorded electroencephalography (EEG) in 114 post-lingually deafened CI users while they completed the California Consonant Test (CCT): a word-in-noise task. In many subjects, data were also collected on two other commonly used clinical measures of speech perception: a word-in-quiet task (Consonant-Nucleus-Consonant [CNC]) word and a sentence-in-noise task (AzBio sentences). Neural activity was assessed at a single vertex electrode (Cz), to maximize generalizability to clinical situations. The N1-P2 complex of event-related potentials (ERPs) at this location were included in multiple linear regression analyses, along with several other demographic and hearing factors as predictors of speech in noise performance. ResultsIn general, there was a good agreement between the scores on the three speech perception tasks. ERP amplitudes did not predict AzBio performance which was predicted by the duration of device use, low-frequency hearing thresholds, and age. However, ERP amplitudes were strong predictors for performance for both word recognition tasks: the CCT (which was conducted simultaneously with EEG recording), and the CNC (conducted offline). These correlations held even after accounting for known predictors of performance including residual low-frequency hearing thresholds. In CI-users, better performance was predicted by an increased cortical response to the target word, in contrast to previous reports in normal-hearing subjects in whom speech perception ability was accounted for by the ability to suppress noise. ConclusionsThese data indicate a neurophysiological correlate of speech-in-noise performance that can be relatively easily captured within the clinic, thereby revealing a richer profile of an individuals hearing performance than shown by psychoacoustic measures alone. These results also highlight important differences between sentence and word recognition measures of performance and suggest that individual differences in these measures may be underwritten by different mechanisms. Finally, the contrast with prior reports of NH listeners in the same task suggests CI-users performance may be explained by a different weighting of neural processes than NH listeners.

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Oscillatory correlates of auditory working memory examined with human electrocorticography

This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in auditory cortex, inferior frontal cortex and the hippocampus using a paradigm with a delay period greater than 10s. The relationship between such BOLD changes and ensemble activity in different frequency bands is complex, and the long delay period raised the possibility that long-term memory mechanisms were engaged. Here we assessed LFPs in different frequency bands in six subjects with recordings from all candidate brain regions using a paradigm with a short delay period of 3 s. Sustained delay activity was demonstrated in all areas, with different patterns in the different areas. Enhancement in low frequency (delta) power and suppression across higher frequencies (beta/gamma) were demonstrated in primary auditory cortex in medial Heschls gyrus (HG) whilst non-primary cortex showed patterns of enhancement and suppression that altered at different levels of the auditory hierarchy from lateral HG to superior- and middle-temporal gyrus. Inferior frontal cortex showed increasing suppression with increasing frequency. The hippocampus and parahippocampal gyrus showed low frequency increases and high frequency decreases in oscillatory activity. The work demonstrates sustained activity patterns that can only be explained by AWM maintenance, with prominent low-frequency increases in medial temporal lobe regions.

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Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Cognitive pathways supporting human language and declarative memory are thought to have uniquely evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-specific effective connectivity between regions important for cognition. We harnessed a new approach using functional imaging to visualize the impact of direct electrical brain stimulation in human neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory cortex to vocalization responsive regions in vlPFC. The results identify a common effective connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the hippocampus (via parahippocampal cortex) in human and nonhuman primates. HighlightsO_LIPrivileged human auditory to inferior frontal connectivity, linked to monkeys C_LIO_LICommon auditory to parahippocampal effective connectivity in both species C_LIO_LIGreater lateralization in human effective connectivity, more symmetrical in monkeys C_LIO_LIHuman fronto-temporal network function rooted in evolutionarily conserved signature C_LI eTOC short summaryFunctional connectivity between regions crucial for language and declarative memory is thought to have substantially differentiated in humans. Using a new technique to similarly visualize directional effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns in both species between fronto-temporal regions crucial for cognition.

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