Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self-initiated stimuli

Actions modulate sensory processing by attenuating responses to self- compared to externally generated inputs, which is traditionally attributed to stimulus-specific motor predictions. Yet, suppression has been also found for stimuli merely coinciding with actions, pointing to unspecific processes that may be driven by neuromodulatory systems. Meanwhile, the differential processing for self-generated stimuli raises the possibility of producing effects also on memory for these stimuli; however, evidence remains mixed as to the direction of the effects. Here, we assessed the effects of actions on sensory processing and memory encoding of concomitant, but unpredictable sounds, using a combination of selfgeneration and memory recognition task concurrently with EEG and pupil recordings. At encoding, subjects performed button presses that half of the time generated a sound (motor auditory; MA) and listened to passively presented sounds (auditory-only; A). At retrieval, two sounds were presented and participants had to respond which one was present before. We measured memory bias and memory performance by having sequences where either both or only one of the test sounds were presented at encoding, respectively. Results showed worse memory performance – but no differences in memory bias –, attenuated responses, and larger pupil diameter for MA compared to A sounds. Critically, the larger the sensory attenuation and pupil diameter, the worse the memory performance for MA sounds. Nevertheless, sensory attenuation did not correlate with pupil dilation. Collectively, our findings suggest that sensory attenuation and neuromodulatory processes coexist during actions, and both relate to disrupted memory for concurrent, albeit unpredictable sounds

Self-generation and sound intensity interactively modulate perceptual bias, but not perceptual sensitivity

The ability to distinguish self-generated stimuli from those caused by external sources is critical for all behaving organisms. Although many studies point to a sensory attenuation of self-generated stimuli, recent evidence suggests that motor actions can result in either attenuated or enhanced perceptual processing depending on the environmental context (i.e., stimulus intensity). The present study employed 2-AFC sound detection and loudness discrimination tasks to test whether sound source (self- or externally-generated) and stimulus intensity (supra- or near-threshold) interactively modulate detection ability and loudness perception. Self-generation did not affect detection and discrimination sensitivity (i.e., detection thresholds and Just Noticeable Difference, respectively). However, in the discrimination task, we observed a significant interaction between self-generation and intensity on perceptual bias (i.e. Point of Subjective Equality). Supra-threshold self-generated sounds were perceived softer than externally-generated ones, while at near-threshold intensities self-generated sounds were perceived louder than externally-generated ones. Our findings provide empirical support to recent theories on how predictions and signal intensity modulate perceptual processing, pointing to interactive effects of intensity and self-generation that seem to be driven by a biased estimate of perceived loudness, rather by changes in detection and discrimination sensitivity

Attentional gain is modulated by probabilistic feature expectations in a spatial cueing task: ERP evidence

Several theoretical and empirical studies suggest that attention and perceptual expectations influence perception in an interactive manner, whereby attentional gain is enhanced for predicted stimuli. The current study assessed whether attention and perceptual expectations interface when they are fully orthogonal, i.e., each of them relates to different stimulus features. We used a spatial cueing task with block-wise spatial attention cues that directed attention to either left or right visual field, in which Gabor gratings of either predicted (more likely) or unpredicted (less likely) orientation were presented. The lateralised posterior N1pc component was additively influenced by attention and perceptual expectations. Bayesian analysis showed no reliable evidence for the interactive effect of attention and expectations on the N1pc amplitude. However, attention and perceptual expectations interactively influenced the frontally distributed anterior N1 component (N1a). The attention effect (i.e., enhanced N1a amplitude in the attended compared to the unattended condition) was observed only for the gratings of predicted orientation, but not in the unpredicted condition. These findings suggest that attention and perceptual expectations interactively influence visual processing within 200 ms after stimulus onset and such joint influence may lead to enhanced endogenous attentional control in the dorsal fronto-parietal attention network

Standard tone stability as a manipulation of precision in the oddball paradigm: Modulation of prediction error responses to fixed-probability deviants

Electrophysiological sensory deviance detection signals, such as the mismatch negativity (MMN), have been interpreted from the predictive coding framework as manifestations of prediction error (PE). From a frequentist perspective of the classic oddball paradigm, deviant stimuli are unexpected because of their low probability. However, the amount of PE elicited by a stimulus can be dissociated from its probability of occurrence: when the observer cannot make confident predictions, any event holds little surprise value, no matter how improbable. Here we tested the hypothesis that the magnitude of the neural response elicited to an improbable sound (D) would scale with the precision of the prediction derived from the repetition of another sound (S), by manipulating repetition stability. We recorded the Electroencephalogram (EEG) from 20 participants while passively listening to 4 types of isochronous pure tone sequences differing in the probability of the S tone (880 Hz) while holding constant the probability of the D tone [1,046 Hz; p(D) = 1/11]: Oddball [p(S) = 10/11]; High confidence (7/11); Low confidence (4/11); and Random (1/11). Tones of 9 different frequencies were equiprobably presented as fillers [p(S) C p(D) C p(F) = 1]. Using a mass-univariate non-parametric, cluster-based correlation analysis controlling for multiple comparisons, we found that the amplitude of the deviant-elicited ERP became more negative with increasing S probability, in a time-electrode window consistent with the MMN (ca. 120- 200 ms; frontal), suggesting that the strength of a PE elicited to an improbable event indeed increases with the precision of the predictive model

COMT and DRD2/ANKK-1 gene-gene interaction account for resetting of gamma neural oscillations to auditory stimulus-driven attention

Attention capture by potentially relevant environmental stimuli is critical for human survival, yet it varies considerably among individuals. A large series of studies has suggested that attention capture may depend on the cognitive balance between maintenance and manipulation of mental representations and the flexible switch between goal-directed representations and potentially relevant stimuli outside the focus of attention; a balance that seems modulated by a prefrontostriatal dopamine pathway. Here, we examined inter-individual differences in the cognitive control of attention through studying the effects of two single nucleotide polymorphisms regulating dopamine at the prefrontal cortex and the striatum (i.e., COMTMet108/158Val and ANKK1/DRD2TaqIA) on stimulus-driven attention capture. Healthy adult participants (N = 40) were assigned to different groups according to the combination of the polymorphisms COMTMet108/158Val and ANKK1/DRD2TaqIA, and were instructed to perform on a well-established distraction protocol. Performance in individuals with a balance between prefrontal dopamine display and striatal receptor density was slowed down by the occurrence of unexpected distracting events, while those with a rather unbalanced dopamine activity were able maintain task performance with no time delay, yet at the expense of a slightly lower accuracy. This advantage, associated to their distinct genetic profiles, was paralleled by an electrophysiological mechanism of phase-resetting of gamma neural oscillation to the novel, distracting events. Taken together, the current results suggest that the epistatic interaction between COMTVal108/158Met and ANKK1/DRD2 TaqIa genetic polymorphisms lies at the basis of stimulus-driven attention capture

Working memory influences on auditory novelty processing in the human brain

[eng] Novel events in the context generate an involuntary orienting response which may have a different impact on the performance of ongoing tasks depending on the specific situation in which humans are immersed. The five studies that form this thesis studied several factors that can modulate responses towards novel sounds and the specific impact that these sounds have on behaviour. This issue was approached measuring the performance of healthy, young individuals on simple visual tasks while they attempted to ignore irrelevant sounds. The auditory stimulation consisted in all cases of a stream of repetitive, equal tones. Occasionally, and in an unpredictable manner, one of these repetitive tones was replaced by an environmental novel sound. In five studies, three different techniques were used to measure brain responses related to novel sounds: event-related potentials (ERP), magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI). In different studies, involuntary orienting towards novel sounds resulted in a disruption or a facilitation of visual task performance. The results of the present studies indicate that novel sounds generate a combined alerting and orienting response. The impact that novel sounds have on behaviour may thus depend on the relative contribution of the alerting and orienting components, which can be determined by the demand of the visual task. However, the same sequence of brain responses was elicited in the present studies by novel sounds irrespective of their behavioural outcomes. We investigated the modulation of brain responses elicited by novel sounds when participants had to perform visual tasks that involved the maintenance of information in working memory (WM). Generally, the results show that in conditions of WM load, the orienting of attention towards novel sounds is diminished. The neurophysiological mechanism underlying diminished orienting was the inhibition of brain responses in auditory cortex and also in inferior frontal cortex, both areas that were involved in the processing of novel sounds. Moreover, the processing of novel stimuli in these areas was not completely abolished, but rather it was attenuated at a late phase, circa 300 ms after the occurrence of the novel sound. At this stage, preattentive change detection processes had been completed in these same areas. Finally, we showed that interference by novel sounds can also be modulated by cognitive control mechanisms. We investigated brain responses to auditory stimuli presented immediately after participants had been distracted by a novel sound. The results showed that, following distraction, sensory responses related to task-relevant, visual information were enhanced in visual cortex, while auditory processing areas were inhibited. The results of these studies have provided further insight into the cerebral mechanisms of attention control, demonstrating specific interactions and mutual modulations between endogenous and exogenous attention.[spa] Los eventos novedosos en el entorno generan una respuesta de orientación involuntaria que puede tener un impacto diferente en el desempeño de las tareas en curso dependiendo de la situación específica en la que los humanos están inmersos. Los cinco estudios que forman esta tesis estudiaron varios factores que pueden modular las respuestas hacia sonidos novedosos y el impacto que estos sonidos tienen sobre la conducta. Esta cuestión se abordó midiendo el rendimiento de sujetos sanos y jóvenes en tareas visuales simples mientras trataban de ignorar sonidos irrelevantes. La estimulación auditiva consistió en todos los casos en una serie de tonos iguales y repetitivos. Ocasionalmente, y de manera impredecible, uno de estos tonos repetitivos se sustituyó por un sonido ambiental novedoso. En cinco estudios, se utilizaron tres técnicas diferentes para medir las respuestas cerebrales relacionadas con los sonidos novedosos: potenciales evocados (PEs), magnetoencefalografía (MEG), y resonancia magnética funcional (RMf). En diferentes estudios, la orientación involuntaria hacia los sonidos novedosos resultó en una disrupción o en una facilitación del rendimiento en la tarea visual. Los resultados de los presentes estudios indican que los sonidos novedosos generan una respuesta combinada de orientación y alerta. El impacto que los sonidos novedosos tienen sobre la conducta puede depender entonces de la contribución relativa de los componentes de alerta y de orientación, que puede venir determinada por las demandas de la tarea visual. Sin embargo, en los presentes estudios, los sonidos novedosos generaron la misma secuencia de respuestas cerebrales con independencia de su impacto sobre la conducta. Hemos investigado la modulación de las respuestas cerebrales generadas por los sonidos novedosos cuando los sujetos tenían que realizar tareas visuales que involucraban el mantenimiento de información en memoria de trabajo (MT). En general, los resultados mostraron que en condiciones de carga en MT, la orientación de la atención hacia los sonidos novedosos está atenuada. El mecanismo neurofisiológico que subyace la atenuación de la orientación fue la inhibición de respuestas cerebrales en el córtex auditivo y también en el córtex frontal inferior, ambas áreas que están implicadas en el procesamiento de los sonidos novedosos. Además, el procesamiento de los sonidos novedosos en estas áreas no se abolió completamente, sino que se atenuó en una fase tardía, alrededor de 300 ms después de la ocurrencia del sonido novedoso. En esta fase, los procesos de detección preatencional del cambio auditivo ya han sido completados en estas mismas áreas. Finalmente, mostramos que la interferencia por los sonidos novedosos también puede modularse por mecanismos de control cognitivo. Investigamos las respuestas cerebrales a estímulos auditivos presentados inmediatamente después de que los sujetos hubiesen sido distraídos por otro sonido novedoso. Los resultados mostraron que, después de la distracción, las respuestas sensoriales relacionadas con la información visual relevante para la tarea se vieron aumentadas en el córtex visual, mientras que las áreas de procesamiento auditivo se inhibieron. Los resultados de estos estudios han proporcionado una mayor comprensión de los mecanismos cerebrales del control de la atención, mostrando interacciones específicas y modulaciones mutuas entre la atención endógena y exógena

Investigació integrada amb EPs i RMf de la interacció entre la memòria de treball i la distracció

Estudi elaborat a partir d’una estada a la University of Wales, Bangor, Regne Unit entre setembre i desembre del 2006. Els sons distractors augmenten el temps de reacció i el nombre de respostes incorrectes en una tasca de classificació visual, demostrant que hi ha distracció conductual durant la realització de la tasca visual. L’enregistrament concomitant de potencials evocats durant la distracció mostra un patró neuroelèctric característic, el potencial de distracció, que es caracteritza per una ona trifàsica. Darrerament, s’ha demostrat que factors “des de dalt” associats al muntatge experimental tindrien una gran influència en els efectes que els estímuls distractors tindrien en la tasca. Estudis recents mostrarien que aquesta resposta d’atenció exògena es pot modular per la càrrega en memòria de treball, reduint-ne la distracció amb la càrrega, fet que contradiu altres dades que mostraven l’efecte oposat. L’objectiu d’aquest estudi ha estat investigar en quines condicions la càrrega en memòria de treball pot exercir un efecte modulador en les respostes conductuals i cerebrals als sons novedosos distractors, i establir la dinàmica espacio-temporal d’aquesta modulació.Report for the scientific sojourn carried out at the University of Wales, Bangor, United Kingdom from September and Desember 2006. Distracting sounds increase the response time and the number of incorrect choices in a visual classification task, revealing behavioural distraction during visual task performance. The concomitant recording of event-related potentials during performance of the distraction reveals a characteristic neuroelectric pattern, the so-called distraction potential, characterized by tri-phasic waveform. However, lately top-down factors associated to the experimental setup have been shown to have a great deal of influence on the effects that distracting stimuli may have on the task. Recent studies would show that this exogenous attention response can be modulated by working memory (WM) load, the distraction being reduced by load, contrasting with data showing opposite effects of WM load on distraction. The purpose of this study was thus to investigate under which conditions working memory load can exert a modulatory effect on the behavioral and brain responses to auditory novel, distracter stimuli, and to establish the spatio-temporal dynamics of such a modulation

COMT and DRD2/ANKK-1 gene-gene interaction account for resetting of gamma neural oscillations to auditory stimulus-driven attention

Attention capture by potentially relevant environmental stimuli is critical for human survival, yet it varies considerably among individuals. A large series of studies has suggested that attention capture may depend on the cognitive balance between maintenance and manipulation of mental representations and the flexible switch between goal-directed representations and potentially relevant stimuli outside the focus of attention; a balance that seems modulated by a prefrontostriatal dopamine pathway. Here, we examined inter-individual differences in the cognitive control of attention through studying the effects of two single nucleotide polymorphisms regulating dopamine at the prefrontal cortex and the striatum (i.e., COMTMet108/158Val and ANKK1/DRD2TaqIA) on stimulus-driven attention capture. Healthy adult participants (N = 40) were assigned to different groups according to the combination of the polymorphisms COMTMet108/158Val and ANKK1/DRD2TaqIA, and were instructed to perform on a well-established distraction protocol. Performance in individuals with a balance between prefrontal dopamine display and striatal receptor density was slowed down by the occurrence of unexpected distracting events, while those with a rather unbalanced dopamine activity were able maintain task performance with no time delay, yet at the expense of a slightly lower accuracy. This advantage, associated to their distinct genetic profiles, was paralleled by an electrophysiological mechanism of phase-resetting of gamma neural oscillation to the novel, distracting events. Taken together, the current results suggest that the epistatic interaction between COMTVal108/158Met and ANKK1/DRD2 TaqIa genetic polymorphisms lies at the basis of stimulus-driven attention capture