Carles Escera

Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change

Behavioral and event-related brain potential (ERP) measures were used to elucidate the neural mechanisms of involuntary engagement of attention by novelty and change in the acoustic environment. The behavioral measures consisted of the reaction time (RT) and performance accuracy (hit rate) in a forced-choice visual RT task where subjects were to discriminate between odd and even numbers. Each visual stimulus was preceded by an irrelevant auditory stimulus, which was randomly either a standard tone (80), a slightly, higher deviant tone (10), or a natural, novel sound (10). Novel sounds prolonged the RT to successive visual stimuli by 17 msec as compared with the RT to visual stimuli that followed standard tones. Deviant tones, in turn, decreased the hit rate but did not significantly affect the RT. In the ERPs to deviant tones, the mismatch negativity (MMN), peaking at 150 msec, and a second negativity, peaking at 400 msec, could be observed. Novel sounds elicited an enhanced N1, with a probable overlap by the MMN, and a large positive P3a response with two different subcomponents: an early centrally dominant P3a, peaking at 230 msec, and a late P3a, peaking at 315 msec with a right-frontal scalp maximum. The present results suggest the involvement of two different neural mechanisms in triggering involuntary attention to acoustic novelty and change: a transient-detector mechanism activated by novel sounds and reflected in the N1 and a stimulus-change detector mechanism activated by deviant tones and novel sounds and reflected in the MMN. The observed differential distracting effects by slightly deviant tones and widely deviant novel sounds support the notion of two separate mechanisms of involuntary attention.

Involuntary attention and distractibility as evaluated with event-related brain potentials

This article reviews recent event-related brain potential (ERP) studies of involuntary attention and distractibility in response to novelty and change in the acoustic environment. These studies show that the mismatch negativity, N1 and P3a ERP components elicited by deviant or novel sounds in an unattended sequence of repetitive stimuli index different processes along the course to involuntary attention switch to distracting stimuli. These studies used new auditory-auditory and auditory-visual distraction paradigms, which enable one to assess objectively abnormal distractibility in several clinical patient groups, such as those suffering from closed-head injuries or chronic alcoholism.

Processing of novel sounds and frequency changes in the human auditory cortex: Magnetoencephalographic recordings

Whole-head magnetoencephalographic (MEG) responses to repeating standard tones and to infrequent slightly higher deviant tones and complex novel sounds were recorded together with event-related brain potentials (ERPs). Deviant tones and novel sounds elicited the mismatch negativity (MMN) component of the ERP and its MEG counterpart (MMNm) both when the auditory stimuli were attended to and when they were ignored. MMNm generators were located bilateral to the superior planes of the temporal lobes where preattentive auditory discrimination appears to occur. A subsequent positive P3a component was elicited by deviant tones and with a larger amplitude by novel sounds even when the sounds were to be ignored. Source localization for the MEG counterpart of P3a (P3am) suggested that the auditory cortex in the superior temporal plane is involved in the neural network of involuntary attention switching to changes in the acoustic environment.

The mismatch negativity (MMN) - A unique window to disturbed central auditory processing in ageing and different clinical conditions

In this article, we review clinical research using the mismatch negativity (MMN), a change-detection response of the brain elicited even in the absence of attention or behavioural task. In these studies, the MMN was usually elicited by employing occasional frequency, duration or speech-sound changes in repetitive background stimulation while the patient was reading or watching videos. It was found that in a large number of different neuropsychiatric, neurological and neurodevelopmental disorders, as well as in normal ageing, the MMN amplitude was attenuated and peak latency prolonged. Besides indexing decreased discrimination accuracy, these effects may also reflect, depending on the specific stimulus paradigm used, decreased sensory-memory duration, abnormal perception or attention control or, most importantly, cognitive decline. In fact, MMN deficiency appears to index cognitive decline irrespective of the specific symptomatologies and aetiologies of the different disorders involved.

Electrical responses reveal the temporal dynamics of brain events during involuntary attention switching

Surviving in the natural environment requires the rapid switching of attention among potentially relevant stimuli. We studied electrophysiologically the involuntary switching time in humans performing a task designed to study brain mechanisms of involuntary attention and distraction (C. Escera et al., 1998, J. Cogn. Neurosci., 10, 590–604). Ten subjects were instructed to discriminate visual stimuli preceded by a task‐irrelevant sound, this being either a repetitive tone (P = 0.8) or a distracting sound, i.e. a slightly higher deviant tone (P = 0.1) or an environmental novel sound (P = 0.1). In different conditions, the sounds preceded the visual stimuli by 245 or 355 ms. Deviant tones and novel sounds prolonged reaction times significantly to subsequent visual stimuli by 7.4 (P < 0.02) and 15.2 ms (P < 0.003), respectively. In addition to a mismatch negativity (MMN) and a positive‐polarity, 320‐ms latency, P3a event‐related potential associated, respectively, with detection of the distracting sound and the subsequent orienting of attention to it, a late frontal negative deflection was observed in distracting trials. The peak latency of this brain response from sound onset was 580 ms in the 245‐ms condition and 115 ms longer in the 355‐ms condition (P < 0.001), peaking consequently at 340 ms from visual stimulus onset, irrespective of the onset of the distracting sound. We suggest that this late frontal negative response may signal over the scalp the process of reallocating attention back to the original task after momentary distraction, and therefore that recovering from distraction may take a similar shifting time as orienting attention involuntarily towards unexpected novelty.

Role of Mismatch Negativity and Novelty-P3 in Involuntary Auditory Attention

It has been proposed that the functional role of the mismatch negativity (MMN) generating process is to issue a call for focal attention toward any auditory change violating the preceding acoustic regularity. This paper reviews the evidence supporting such a functional role and outlines a model of how the attentional system controls the flow of bottom-up auditory information with regard to ongoing-task demands to organize goal-oriented behavior. Specifically, the data obtained in auditory-auditory and auditory-visual distraction paradigms demonstrated that the unexpected occurrence of deviant auditory stimuli or novel sounds captures attention involuntarily, as they distract current task performance. These data indicate that such a process of distraction takes place in three successive stages associated, respectively, to MMN, P3a/novelty-P3, and reorienting negativity (RON), and that the latter two are modulated by the demands of the task at hand.

Task Switching and Novelty Processing Activate a Common Neural Network for Cognitive Control

The abrupt onset of a novel event captures attention away from, and disrupts, ongoing task performance. Less obvious is that intentional task switching compares with novelty-induced behavioral distraction. Here we explore the hypothesis that intentional task switching and attentional capture by a novel distracter both activate a common neural network involved in processing contextual novelty [Barcelo, F., Periez, J. A., & Knight, R. T. Think differently: A brain orienting response to task novelty. NeuroReport, 13, 18871892, 2002.]. Event-related potentials were recorded in two task-cueing paradigms while 16 subjects sorted cards following either two (color or shape; two-task condition) or three (color, shape, or number; three-task condition) rules of action. Each card was preceded by a familiar tone cueing the subject either to switch or to repeat the previous rule. Novel sound distracters were interspersed in one of two blocks of trials in each condition. Both novel sounds and task-switch cues impaired responses to the following visual target. Novel sounds elicited novelty P3 potentials with their usual peak latency and frontal-central scalp distribution. Familiar tonal switch cues in the three- and two-task conditions elicited brain potentials with a similar latency and morphology as the novelty P3, but with relatively smaller amplitudes over frontal scalp regions. Covariance and principal component analyses revealed a sustained frontal negative potential that was distorting concurrent novelty P3 activity to the tonal switch cues. When this frontal negativity was statistically removed, P3 potentials to novel sounds and task-switch cues showed similar scalp topographies. The degree of activation in the novelty P3 network seemed to be a function of the information (entropy) conveyed by the eliciting stimulus for response selection, over and above its relative novelty, probability of occurrence, task relevance, or feedback value. We conclude that novelty P3 reflects transient activation in a neural network involved in updating task set information for goal-directed action selection and might thus constitute one key element in a central bottleneck for attentional control.

The accuracy of sound duration representation in the human brain determines the accuracy of behavioural perception

In recent years, the links between neural activity and perception have been an area of interest in cognitive neuroscience. Combined psychophysiological and psychophysical experiments provide a new powerful tool for establishing the relationship between neural activity and perceptual performance. In animals, intracellular recordings combined with psychophysical detection indices have revealed that a particular neuron or set of neurons can play a critical role in the generation of a perceptual event, showing detection functions (referred to as neurometric functions) which are remarkably similar to psychophysical detection functions, or psychometric functions ( Parker & Newsome, (1998) Annu. Rev. Neurosci., 21, 227–277). As noninvasive techniques for recording neural activity are now available, studies combining neuroelectric and psychophysical measures in humans are sparse. In the present study, the accuracy of the human brain in detecting differences in sound duration and the subjects ability to perceive the same differences were tested by means of mismatch negativity (MMN) and the distance between the distributions of false alarms and hits (sensitivity index d′), respectively. It was found that the accuracy of the human auditory system to represent sound duration information is related to the duration context in which the sounds are heard, and that these contextual representations determine the accuracy of perception at the behavioural level.

The mismatch negativity: an index of cognitive decline in neuropsychiatric and neurological diseases and in ageing

Cognitive impairment is a core element shared by a large number of different neurological and neuropsychiatric diseases. Irrespective of their different aetiologies and symptomatologies, most appear to converge at the functional deficiency of the auditory-frontal cortex network of auditory discrimination, which indexes cognitive impairment shared by these abnormalities. This auditory-frontal cortical deficiency, and hence cognitive decline, can now be objectively measured with the mismatch negativity and its magnetic equivalent. The auditory-frontal cortical network involved seems, therefore, to play a pivotal, unifying role in the different abnormalities. It is, however, more likely that the dysfunction that can be detected with the mismatch negativity and its magnetoencephalographic equivalent manifests a more widespread brain disorder, namely, a deficient N-methyl-D-aspartate receptor function, shared by these abnormalities and accounting for most of the cognitive decline.

Attention capture by auditory significant stimuli: semantic analysis follows attention switching.

Event‐related potentials (ERPs) were recorded from the scalp to investigate a long‐standing controversy in auditory attention research, namely when the ‘breakthrough of the unattended’ takes place in the human brain. Nine subjects classified visual stimuli appearing 300 ms after task‐irrelevant standard tones (80%, i.e. P = 0.8) or novel sounds (20%, i.e. P = 0.2) into odd/even categories. After the recording session, subjects scored the novel sounds as to whether they had any particular meaning (identifiable) or were perceived as a burst of noise (non‐identifiable), and performance and ERPs were analysed according to this classification. A control condition, in which the visual stimuli were presented with no sounds, showed that subjects covertly monitored the task‐irrelevant sounds during visual task‐performance, and a further condition, in which the auditory and visual stimuli appeared regardless of each other, made it possible to trace the processing of the distracters during allocation of attention outside the auditory environment. Results yielded identical N1‐enhancement for the two types of novel sounds, indicating similar attention switching triggered to these two types of unexpected sounds. However, there was a stronger orientating of attention towards identifiable novel sounds, as indicated both by behavioural distraction and by larger novelty‐P3. Furthermore, this stronger orientating of attention was due to the sounds being contingent on the visual stimuli, as no increase in novelty‐P3 to identifiable novel sounds was observed in the control condition, in which the sounds occurred outside the attentional set. Therefore, provided that the N1‐enhancement reflects a call for focal attention, and novelty‐P3 the effective orientating of attention towards the eliciting sounds, the present results suggest that semantic analysis of significant sounds occurs after a transitory switch of attention towards the eliciting stimuli. Moreover, as the novelty‐P3 increase in amplitude was observed only when subjects covertly monitored the sounds, the present data suggest that semantic analysis of irrelevant sounds depends on the top‐down cognitive influences of the attentional set.