Auditory Detection Research Articles

Dissociating temporal attention from spatial attention and motor response preparation: A high-density EEG study

Engagement of various forms of attention and response preparation determines behavioral performance during stimulus–response tasks. Many studies explored the respective properties and neural signatures of each of these processes. However, very few experiments were conceived to explore their interaction. In the present work we used an auditory target detection task during which both temporal attention on the one side, and spatial attention and motor response preparation on the other side could be explicitly cued. Both cueing effects speeded response times, and showed strictly additive effects. Target ERP analysis revealed modulations of N1 and P3 responses by these two forms of cueing. Cue–target interval analysis revealed two main effects paralleling behavior. First, a typical contingent negative variation (CNV), induced by the cue and resolved immediately after target onset, was found larger for temporal attention cueing than for spatial and motor response cueing. Second, a posterior and late cue-P3 complex showed the reverse profile. Analyses of lateralized readiness potentials (LRP) revealed both patterns of motor response inhibition and activation. Taken together these results help to clarify and disentangle the respective effects of temporal attention on the one hand, and of the combination of spatial attention and motor response preparation on the other hand on brain activity and behavior.

Post-release habitat utilisation by Francolinus bicalcaratus ayesha, a critically endangered subspecies endemic to Morocco: implications for optimising future release programmes

SummaryCharacterising the habitat use of released captive-bred birds is required to help optimise future avian reintroduction programmes. The critically endangered Double-spurred Francolin Francolinus bicalcaratus ayesha is endemic to north-west Morocco, where it inhabits forests of cork oak Quercus suber. To improve the viability of this threatened population, 300 captive-bred francolins were released into a game reserve, and post-release monitoring was conducted. This study aimed to identify habitat variables determining the habitat selection of the Double-spurred Francolin. Auditory detection was used during transect surveys of calling males to locate birds and their habitat occupation. Comparison of occupied and random plots showed that this bird is found mostly in flat topography with high cover of shrubs and dense cork oak trees, and close to the release site and water points. Conservation of Double-spurred Francolin depends on the choice of the release point within the cork oak forest, which should be in proximity to suitable cover of cork oak trees, shrubs and water points. Such choices would allow a rapid adaptation to prevailing conditions within release sites. Further multi-scale studies are needed to improve our understanding of the effects of ecological factors on the processes of habitat selection by this endemic subspecies.

Rapid Task-Related Plasticity of Spectrotemporal Receptive Fields in the Auditory Midbrain.

Previous research has demonstrated that auditory cortical neurons can modify their receptive fields when animals engage in auditory detection tasks. We tested for this form of task-related plasticity in the inferior colliculus (IC) of ferrets trained to detect a pure tone target in a sequence of noise distractors that did not overlap in time. During behavior, responses were suppressed at the target tone frequency in approximately half of IC neurons relative to the passive state. This suppression often resulted from a combination of a local tuning change and a global change in overall excitability. Local and global suppression were stronger when the target frequency was aligned to neuronal best frequency. Local suppression in the IC was indistinguishable from that described previously in auditory cortex, while global suppression was unique to the IC. The results demonstrate that engaging in an auditory task can change selectivity for task-relevant features in the midbrain, an area where these effects have not been reported previously. Significance statement: Previous studies have demonstrated that the receptive fields of cortical neurons are modified when animals engage in auditory behaviors, a process that is hypothesized to provide the basis for segregating sound sources in an auditory scene. This study demonstrates for the first time that receptive fields of neurons in the midbrain inferior colliculus are also modified during behavior. The magnitude of the tuning changes is similar to previous reports in cortex. These results support a hierarchical model of behaviorally driven sound segregation that begins in the subcortical auditory network.

Can new paradigms bring new perspectives for mismatch negativity studies in schizophrenia?

Attenuation of mismatch negativity (MMN), event-related potential (ERP) that assess dysfunction in auditory change detection, is a robust finding in schizophrenia. Most studies on MMN in schizophrenia use a two-tone paradigm in which the deviant sound has a different duration or frequency. Because this oddball paradigm has provided consistent results over time and has proven to be a reliable research tool, it dominates this area of research. Over twenty years of investigation into MMN in schizophrenia have shown that change in any of the characteristics of stimulation results in MMN; however there is surprisingly little evidence on MMN in schizophrenia from studies using stimulation other than the typical oddball paradigm. In this paper we focus on studies which have assessed auditory change discrimination in schizophrenia employing paradigms other than a typical oddball. We also briefly discuss research on visual MMN in schizophrenia. The aim was to highlight how research using new paradigms has added to understanding of MMN in schizophrenia. In conclusion we discuss stimulation which could be useful for future research on MMN in schizophrenia.

An auditory feature detection circuit for sound pattern recognition.

From human language to birdsong and the chirps of insects, acoustic communication is based on amplitude and frequency modulation of sound signals. Whereas frequency processing starts at the level of the hearing organs, temporal features of the sound amplitude such as rhythms or pulse rates require processing by central auditory neurons. Besides several theoretical concepts, brain circuits that detect temporal features of a sound signal are poorly understood. We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song. The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide. This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.

On the Cognitive Demands of Different Controller Dynamics

The cognitive workload of a steering task could reflect its demand on attentional as well as working memory resources under different conditions. These respective demands could be differentiated by evaluating components of the event-related potential (ERP) response to different types of stimulus probes, which are claimed to reflect the availability of either attention (i.e., novelty-P3) or working memory (i.e., target-P3) resources. Here, a within-subject analysis is employed to evaluate the robustness of ERP measurements in discriminating the cognitive demands of different steering conditions. We find that the amplitude of novelty-P3 ERPs to task-irrelevant environmental sounds is diminished when participants are required to perform a steering task. This indicates that steering places a demand on attentional resources. In addition, target-P3 ERPs to a secondary auditory detection task vary when the controller dynamics in the steering task are manipulated. This indicates that differences in controller dynamics vary in their working memory demands.

Attention deficits revealed by passive auditory change detection for pure tones and lexical tones in ADHD children.

Inattention (IA) has been a major problem in children with attention deficit/hyperactivity disorder (ADHD), accounting for their behavioral and cognitive dysfunctions. However, there are at least three processing steps underlying attentional control for auditory change detection, namely pre-attentive change detection, involuntary attention orienting, and attention reorienting for further evaluation. This study aimed to examine whether children with ADHD would show deficits in any of these subcomponents by using mismatch negativity (MMN), P3a, and late discriminative negativity (LDN) as event-related potential (ERP) markers, under the passive auditory oddball paradigm. Two types of stimuli—pure tones and Mandarin lexical tones—were used to examine if the deficits were general across linguistic and non-linguistic domains. Participants included 15 native Mandarin-speaking children with ADHD and 16 age-matched controls (across groups, age ranged between 6 and 15 years). Two passive auditory oddball paradigms (lexical tones and pure tones) were applied. The pure tone oddball paradigm included a standard stimulus (1000 Hz, 80%) and two deviant stimuli (1015 and 1090 Hz, 10% each). The Mandarin lexical tone oddball paradigm’s standard stimulus was /yi3/ (80%) and two deviant stimuli were /yi1/ and /yi2/ (10% each). The results showed no MMN difference, but did show attenuated P3a and enhanced LDN to the large deviants for both pure and lexical tone changes in the ADHD group. Correlation analysis showed that children with higher ADHD tendency, as indexed by parents’ and teachers’ ratings on ADHD symptoms, showed less positive P3a amplitudes when responding to large lexical tone deviants. Thus, children with ADHD showed impaired auditory change detection for both pure tones and lexical tones in both involuntary attention switching, and attention reorienting for further evaluation. These ERP markers may therefore be used for the evaluation of anti-ADHD drugs that aim to alleviate these dysfunctions.

Attention Wins over Sensory Attenuation in a Sound Detection Task.

‘Sensory attenuation’, i.e., reduced neural responses to self-induced compared to externally generated stimuli, is a well-established phenomenon. However, very few studies directly compared sensory attenuation with attention effect, which leads to increased neural responses. In this study, we brought sensory attenuation and attention together in a behavioural auditory detection task, where both effects were quantitatively measured and compared. The classic auditory attention effect of facilitating detection performance was replicated. When attention and sensory attenuation were both present, attentional facilitation decreased but remained significant. The results are discussed in the light of current theories of sensory attenuation.

Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback

Basal forebrain cholinergic neurons constitute a major neuromodulatory system implicated in normal cognition and neurodegenerative dementias. Cholinergic projections densely innervate neocortex, releasing acetylcholine to regulate arousal, attention, and learning. However, their precise behavioral function is poorly understood because identified cholinergic neurons have never been recorded during behavior. To determine which aspects of cognition their activity might support, we recorded cholinergic neurons using optogenetic identification in mice performing an auditory detection task requiring sustained attention. We found that a non-cholinergic basal forebrain population-but not cholinergic neurons-were correlated with trial-to-trial measures of attention. Surprisingly, cholinergic neurons responded to reward and punishment with unusual speed and precision (18 ± 3ms). Cholinergic responses were scaled by the unexpectedness of reinforcement and were highly similar across neurons and two nuclei innervating distinct cortical areas. These results reveal that the cholinergic system broadcasts a rapid and precisely timed reinforcement signal, supporting fast cortical activation and plasticity.

Mismatch negativity in tobacco-naïve cannabis users and its alteration with acute nicotine administration

Chronic cannabis use may interact with factors, such as age of onset of cannabis use, family history, and genetic factors, to elicit schizophrenia (SZ)-like symptoms, including sensory and cognitive deficits. However, evidence of a relationship between cannabis use and cognitive impairment is confounded by concomitant use of tobacco. The objective of this study was to compare tobacco-naïve cannabis users with individuals without a history of tobacco/cannabis use on the auditory mismatch negativity (MMN) event-related potential (ERP), a neural measure of auditory deviance detection which is diminished in SZ. An exploratory arm of the study, conducted within a randomized, double-blind, placebo controlled design, examined the acute effects of nicotine gum (6mg) on MMN in cannabis users. MMN was recorded in response to 5 deviant stimuli within an optimal MMN paradigm in 44 healthy, non-tobacco smoking volunteers aged 18–26. Cannabis users (n=21) started smoking cannabis prior to age 17, at least 1 joint per month. To examine the effects of chronicity, users were grouped into relatively heavy long-term (HLT; n=11) users and light short-term (LST; n=10) users. Impaired deviance detection was shown in cannabis users vs. nonusers as reflected by a smaller MMN to duration deviants. Chronicity of use was also associated with MMN alterations, as HLTs displayed a reduced duration and gap MMN vs. LSTs. Compared with placebo, nicotine treatment enhanced select MMN deviants in cannabis user subgroups. As deficits associated with early and persistent cannabis use are similar to those seen in SZ, these dose-dependant disturbances in early sensory processing with cannabis use may be one cognitive pathway which mediates an increased risk for SZ in vulnerable youth, and be influenced by concurrent cigarette smoking behavior.

A frontal attention mechanism in the visual mismatch negativity

Automatic detection of environmental change is a core component of attention. The mismatch negativity (MMN), an electrophysiological marker of this mechanism, has been studied prominently in the auditory domain, with cortical generators identified in temporal and frontal regions. Here, we combined electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) to assess whether the underlying frontal regions associated with auditory change detection also play a role in visual change detection. Twenty healthy young adults completed a visual MMN task in separate EEG and fMRI sessions. Region of interest analyses were conducted on left and right middle frontal (MFG) and inferior frontal (IFG) gyri, i.e., the frontal areas identified as potential auditory MMN generators. A significant increase in activation was observed in the left IFG and MFG in response to blocks containing deviant stimuli. These findings suggest that a frontal mechanism is involved in the detection of change in the visual MMN. Our results support the notion that frontal mechanisms underlie attention switching, as measured via MMN, across multiple modalities.

Stimulus-specific adaptation in the inferior colliculus: The role of excitatory, inhibitory and modulatory inputs

Patients suffering from pathologies such as schizophrenia, depression or dementia exhibit cognitive impairments, some of which can be reflected in event-related potential (ERP) measurements as the mismatch negativity (MMN). The MMN is one of the most commonly used ERPs and provides an electrophysiological index of auditory change or deviance detection. Moreover, MMN has been positioned as a potentially promising biomarker candidate for the diagnosis and prediction of the outcome of schizophrenia. Dysfunction of neural receptors has been linked to the etiopathology of schizophrenia or the induction of psychophysiological anomalies similar to those observed in schizophrenia. Stimulus-specific adaptation (SSA) is a neural mechanism that contributes to the upstream processing of auditory change detection. Auditory neurons that exhibit SSA specifically adapt their response to repetitive sounds but maintain their excitability to respond to rare ones. Thus, by studying the role of neuronal receptors on SSA, we can contribute to detangle the cellular bases of the impairments in deviance processing occurring in mental pathologies. Here, we review the current knowledge on the effect of GABAA-mediated inhibition and the modulation of acetylcholine on SSA in the inferior colliculus, and we add unpublished original data obtained blocking glutamate receptors. We found that the blockade of GABAA and glutamate receptors mediates an overall increase or decrease of the neural response, respectively, while acetylcholine affects only the response to the repetitive sounds. These results demonstrate that GABAergic, glutamatergic and cholinergic receptors play different and complementary roles on shaping SSA.

V21. Electrophysiological correlates of auditory change detection: A simultaneous depth and scalp EEG study

Introduction Attentive monitoring of the environment is fundamental for efficient detection of relevant stimuli and is well investigated for cortical regions. However, subcortical network circuitry and the involvement of these structures in the context of detection of relevant stimuli, involuntary attention and distractibility is not well understood. The P300 component is frequently used in electroencephalographic (EEG) studies as a measure for attentional and cognitive functions and is supposed to give further insight into context-specific processes of subcortical structures. Methods In this ongoing study, simultaneous recordings of local field potentials (LFPs) and event-related potentials (ERPs) from scalp EEG were obtained in 14 patients (mean age = 51.6 ± 21.7 years) undergoing deep brain stimulation (DBS). These patients were implanted bilaterally with quadripolar electrodes in the subthalamic nucleus (STN; n = 5; Parkinson disease), the thalamic ventral intermediate nucleus (VIM; n = 5; essential tremor and cervical dystonia), or the globus pallidus internus (GPi; n = 4; segmental dystonia, Parkinson disease and Tourette syndrome). Within five days after surgery, patients performed an auditory three-class oddball paradigm with externalized DBS electrodes. ERPs from scalp and DBS electrodes were analyzed upon presentation of one frequent standard stimulus (900 Hz; 72%) and two infrequent stimuli, either being a relevant (1200 Hz; 14%) or a distractor (600 Hz; 14%) stimulus. Stimuli were presented for 62 ms with an interstimulus interval of 800–1200 ms. The patients were asked to press a button to the relevant stimulus. Results Analysis reveals high accuracy in all patients (84.25%±15.14). Preliminary EEG results show a P300 component over parietal regions that was largest upon presentation of target stimuli compared with distractor and standard stimuli. A similar P300-like component was also found in depth recordings, suggesting stimulus-specific responses of subcortical structures. Here, STN showed shorter latencies and larger amplitudes compared to GPi or Vim. Discussion The P300 reflects attentional processes that require stimulus detection and discrimination. The present results suggest that, in particular, the STN may play a pivotal role in context-specific processes.

Behavioral State—Getting “In The Zone”

In this issue of Neuron, McGinley etal. (2015) investigate a classic observation from psychology linking arousal state with behavioral performance, demonstrating neural correlates of an "optimal" state for an auditory detection task.

Ongoing dynamics in large-scale functional connectivity predict perception

Most brain activity occurs in an ongoing manner not directly locked to external events or stimuli. Regional ongoing activity fluctuates in unison with some brain regions but not others, and the degree of long-range coupling is called functional connectivity, often measured with correlation. Strength and spatial distributions of functional connectivity dynamically change in an ongoing manner over seconds to minutes, even when the external environment is held constant. Direct evidence for any behavioral relevance of these continuous large-scale dynamics has been limited. Here, we investigated whether ongoing changes in baseline functional connectivity correlate with perception. In a continuous auditory detection task, participants perceived the target sound in roughly one-half of the trials. Very long (22-40 s) interstimulus intervals permitted investigation of baseline connectivity unaffected by preceding evoked responses. Using multivariate classification, we observed that functional connectivity before the target predicted whether it was heard or missed. Using graph theoretical measures, we characterized the difference in functional connectivity between states that lead to hits vs. misses. Before misses compared with hits and task-free rest, connectivity showed reduced modularity, a measure of integrity of modular network structure. This effect was strongest in the default mode and visual networks and caused by both reduced within-network connectivity and enhanced across-network connections before misses. The relation of behavior to prestimulus connectivity was dissociable from that of prestimulus activity amplitudes. In conclusion, moment to moment dynamic changes in baseline functional connectivity may shape subsequent behavioral performance. A highly modular network structure seems beneficial to perceptual efficiency.

Multisensory Competition Is Modulated by Sensory Pathway Interactions with Fronto-Sensorimotor and Default-Mode Network Regions.

Multisensory information competes for preferential access to consciousness. It remains unknown what neural processes cause one particular modality to win multisensory competition and eventually dominate behavior. Thus, in a paradigm in which human participants sought to make simultaneous auditory and visual detection responses, we sought to identify prestimulus and poststimulus neural signals that were associated with auditory and visual dominance on each trial. Behaviorally, visual detection responses preceded auditory responses more frequently than vice versa. Even when visual responses were preceded by auditory responses, they recovered more quickly from previous responses, indicating the dominance of vision over audition. Neurally, visual precedence was associated with increased prestimulus activity in the prefrontal cortex and reduced prestimulus activity in the default-mode network, and increased poststimulus connectivity between the prefrontal cortex and the visual system. Moreover, the dorsal visual stream showed not only increased activity in post-perceptual phases but also enhanced connectivity with the sensorimotor cortex, indicating the functional role of the dorsal visual stream in prioritizing the flow of visual information into the motor system. In contrast, auditory precedence was associated with increased prestimulus activity in the auditory cortex and increased poststimulus neural coupling between the auditory and the sensorimotor cortex. Finally, whenever one modality lost multisensory competition, the corresponding sensory cortex showed enhanced connectivity with the default-mode network. Overall, the outcome of audiovisual competition depended on dynamic interactions between sensory systems and both the fronto-sensorimotor and the default-mode network. Together, these results revealed both the neural causes and the neural consequences of visual and auditory dominance during multisensory competition.

Finding the missing-stimulus mismatch negativity (MMN) in early psychosis: Altered MMN to violations of an auditory gestalt

The mismatch negativity (MMN) is an EEG-derived event-related potential (ERP) elicited by any violation of a predicted auditory ‘rule’, regardless of whether one is attending to the stimuli, and is thought to reflect updating of the stimulus context. Chronic schizophrenia patients exhibit robust MMN deficits, while MMN reduction in first-episode and early phase psychosis is significantly less consistent. Traditional two-tone “oddball” MMN measures of sensory information processing may be considered too simple for use in early phase psychosis in which pathology has not progressed fully, and a paradigm that probes higher order processes may be more appropriate for elucidating auditory change detection deficits. This study investigated whether MMN deficits could be detected in early phase psychosis (EP) patients using an abstract ‘missing stimulus’ pattern paradigm (Salisbury, 2012).The stimuli were 400 groups of six tones (1000Hz, 50ms duration, 330ms stimulus onset asynchrony), which was presented with an inter-trial interval of 750ms. Occasionally a group contained a deviant, meaning that it was missing either the 4th or 6th tone (50 trials each). EEG recordings of 13 EP patients (≤5year duration of illness) and 15 healthy controls (HC) were collected. Patients and controls did not significantly differ on age or years of education.Analyses of MMN amplitudes elicited by missing stimuli revealed amplitude reductions in EP patients, suggesting that these deficits are present very early in the progression of the illness. While there were no correlations between MMN measures and measures such as duration of illness, medication dosage or age, MMN amplitude reductions were correlated with positive symptomatology (i.e. auditory hallucinations).These findings suggest that MMNs elicited by the ‘missing stimulus’ paradigm are impaired in psychosis patients early in the progression of illness and that previously reported MMN-indexed deficits related to auditory hallucinations in chronic patients may also be present in EP patients. As such, this paradigm may have promise in identifying early processing deficits in this population.

Cross-modal cueing in audiovisual spatial attention.

Visual processing is most effective at the location of our attentional focus. It has long been known that various spatial cues can direct visuospatial attention and influence the detection of auditory targets. Cross-modal cueing, however, seems to depend on the type of visual cue: facilitation effects have been reported for endogenous visual cues while exogenous cues seem to be mostly ineffective. In three experiments, we investigated cueing effects on the processing of audiovisual signals. In Experiment 1, we used endogenous cues to investigate their effect on the detection of auditory, visual, and audiovisual targets presented with onset asynchrony. Consistent cueing effects were found in all target conditions. In Experiment 2, we used exogenous cues and found cueing effects only for visual target detection, but not auditory target detection. In Experiment 3, we used predictive exogenous cues to examine the possibility that cue-target contingencies were responsible for the difference between Experiment 1 and 2. In all experiments, we investigated whether a response time model can explain the data and tested whether the observed cueing effects were modality-dependent. The results observed with endogenous cues imply that the perception of multisensory signals is modulated by a single, supramodal system operating in a top-down manner (Experiment 1). In contrast, bottom-up control of attention, as observed in the exogenous cueing task of Experiment 2, mainly exerts its influence through modality-specific subsystems. Experiment 3 showed that this striking difference does not depend on contingencies between cue and target.

An acute dose, randomized trial of the effects of CDP-Choline on Mismatch Negativity (MMN) in healthy volunteers stratified by deviance detection level

Alpha 7 nicotinic acetylcholine receptors (α7 nAChR) are prioritized molecular targets for the development of new pharmacological treatments for impaired cognition in schizophrenia. The use of schizophrenia-associated biomarkers both as endpoints and for segmentation of homogeneous populations for early detection of cognitive enhancing agents has been advanced to enhance the drug discovery process. In this study, the mismatch negativity (MMN) event-related brain potential (ERP), considered one of the few fully developed biomarkers in schizophrenia, was employed: a) to stratify 24 healthy volunteers into subgroups exhibiting low, medium, or high auditory sensory discrimination based on pre-attentive detection of deviant auditory features, and b) to assess their acute response to a low (500 mg) and moderate dose (1000 mg) of CDP-choline, a dietary supplement with selective agonist actions at α7 nAChRs. No significant whole group effects were observed with CDP-choline, and MMN changes were observed only with analysis of subgroups. The effects of CDP-choline interacted both with deviant type and auditory deviance detection level, with individuals exhibiting low MMNs showing enhanced amplitudes, while those with high MMNs evidenced reduced amplitudes with acute dosing of CDP-choline. These preliminary findings of improved auditory deviance detection with CDP-choline in our biomarker-defined healthy surrogate group supports the contention that α7 nicotinic cholinergic agonism be studied as a potential pro-cognitive mechanism in patients with schizophrenia.

Auditory cortical and hippocampal local-field potentials to frequency deviant tones in urethane-anesthetized rats: An unexpected role of the sound frequencies themselves

The human brain can automatically detect auditory changes, as indexed by the mismatch negativity of event-related potentials. The mechanisms that underlie this response are poorly understood. We recorded primary auditory cortical and hippocampal (dentate gyrus, CA1) local-field potentials to serial tones in urethane-anesthetized rats. In an oddball condition, a rare (deviant) tone (p=0.11) randomly replaced a repeated (standard) tone. The deviant tone was either lower (2200, 2700, 3200, 3700Hz) or higher (4300, 4800, 5300, 5800Hz) in frequency than the standard tone (4000Hz). In an equiprobability control condition, all nine tones were presented at random (p=0.11). Differential responses to deviant tones relative to the standard tone were found in the auditory cortex and the dentate gyrus but not in CA1. Only in the dentate gyrus, the responses were found to be standard- (i.e., oddball condition-) specific. In the auditory cortex, the sound frequencies themselves sufficed to explain their generation. These findings tentatively suggest dissociation among non-contextual afferent, contextual afferent and auditory change detection processes. Most importantly, they remind us about the importance of strict control of physical sound features in mismatch negativity studies in animals.