Kimmo Alho

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.

Auditory frequency discrimination and event-related potentials

Auditory stimulus blocks were presented to 6 subjects. 80% of the stimuli in each block were standards of 1000 Hz and 20% were deviants of either 1002 Hz, 1004 Hz, 1008 Hz, 1016 Hz or 1032 Hz, one deviant type in each block. The constant interstimulus interval was 1 sec and the order of the stimuli was randomized. The subject was instructed either to ignore the deviant stimuli (ignore condition) or to press a response key to them (discrimination condition). In the ignore condition, an ERP component called the mismatch negativity (MMN), with a peak latency of approximately 170 msec, was elicited by those deviants exceeding the discrimination threshold (1016 Hz and 1032 Hz) and also those at the threshold (1008 Hz) tended to elicit a small MMN. In the discrimination condition, in addition to MMN, another negative component, N2b, was elicited by the detected deviants. This component had a somewhat longer latency than, and its midline distribution was posterior to, the MMN. The present results are in line with the hypothesis according to which the MMN component reflects the activation of cerebral mechanisms of passive discrimination, those which cause us to become aware of occasional changes in unattended stimulus sequences. In the discrimination condition, N2b and the slow parietal positivity were dominant features of the ERPs elicited by the detected suprathreshold deviants. The data obtained at the discrimination threshold specifically associate the parietal positivity with becoming aware of stimulus change since those deviants which were detected elicited this positivity whereas there was none to those (physically identical) deviants which remained undetected.

Cerebral generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound changes.

Infrequent (“deviant”) sounds occurring in a sequence of repetitive (“standard”) sounds elicit an event-related brain potential (ERP) response called the mismatch negativity (MMN) even in the absence of attention to these sounds. MMN appears to be caused by a neuronal mismatch between the deviant auditory input and a sensory-memory trace representing the standard stimuli. This automatic mismatch process has presumably a central role in discrimination of changes in the acoustic environment outside the focus of attention. Thus, localizing cerebral generators of MMN might help identify brain mechanisms of auditory sensory memory and involuntary attention. This review summarizes results from studies aimed at localizing MMN generators on the basis of (1) scalp-distribution, (2) magnetoencephalographic (MEG), (3) intracranial, and (4) brain-lesion data. These studies indicate that a major MMN source is located in the auditory cortex. However, the exact location of this MMN generator appears to depend on which feature of a sound is changed (e.g., frequency, intensity, or duration), as well as on the complexity of the sound (e.g., a simple tone versus complex sound). Consequently, memory traces for different acoustic features, as well as for sounds of different complexity, might be located in different regions of auditory cortex. However, MMN appears to have generators in other brain structures, too. There is some evidence for contribution of frontal-lobe activity to the MMN, which might be related to the involuntary switching of attention to a stimulus change occurring outside the focus of attention. In addition, intracranial MMN recordings in animals suggest that at least in some species, MMN subcomponents also may be generated in the thalamus and hippocampus.

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.

Responses of the primary auditory cortex to pitch changes in a sequence of tone pips: Neuromagnetic recordings in man

Auditory evoked magnetic fields of the human brain were recorded with a four-channel 1st order gradiometer. Pitch deviance in a sequence of repetitive tone pips elicited magnetic evoked-response changes with a topography suggesting that a neuronal mismatch process to the deviant tones activates the primary auditory cortex.

Separate Time Behaviors of the Temporal and Frontal Mismatch Negativity Sources

It has been proposed that mismatch negativity (MMN) is generated by temporal and frontal lobe sources, the former being associated with change detection and the latter with involuntary switching of attention to sound change. If this switching of attention is triggered by the temporal cortex change-detection mechanism, one would expect that the frontal component of MMN is activated later than the temporal one. This was studied by using 64-channel electroencephalography (EEG) and 122-channel magnetoencephalography (MEG) with realistically shaped head models to determine the source current distribution in different lobes as a function of time. Minimum-norm estimation (MNE) was performed, constraining the solution to the reconstructed cortical sheet. The results support the hypothesis that the frontal MMN generator is activated later than the auditory cortex generator.

Intermodal selective attention. II. Effects of attentional load on processing of auditory and visual stimuli in central space

The effect of processing load on event-related brain potentials (ERPs) was investigated in an intermodal selective attention task in which subjects attended selectively to auditory or visual stimuli. Processing load was manipulated by requiring subjects to detect either difficult-to-detect (deviant) or easy-to-detect (DEVIANT) targets in separate blocks of trials. Attention to auditory stimuli was associated with negative (Nda, 90-170 msec) and positive (Pda, 190-270 msec) enhancements in the ERPs to auditory stimuli. The Nda increased in amplitude with increasing processing load. Deviant auditory stimuli occurring among auditory standard stimuli elicited frontally distributed mismatch negativities (MMNs). The MMN persisted during visual attention and was unaffected by visual processing load. However, the MMN to deviants but not DEVIANTS was enhanced in amplitude with auditory attention. Attention to visual stimuli resulted in positive (Pdv, latency 70-130 msec) and negative (Ndv, 170-270 msec) modulations of visual ERPs, that increased with increasing processing load. Prominent visual deviance-related negativities were observed at occipital and infero-temporal scalp sites (latencies 90-290 msec), but only to DEVIANT visual stimuli. The early MMN-like portion of the visual deviance-related negativity was independent of attention, with equal amplitudes during different auditory and visual conditions.

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.

Right hemisphere dominance of different mismatch negativities

Auditory stimulus blocks were presented to 10 reading subjects. Each block consisted of 2 types of stimulus, standard (P = 90%) and deviant (P = 10%), delivered in a random order with short constant inter-stimulus intervals. The standard stimuli were 600 Hz. 80 dB SPL 50 msec sine wave bursts. In different blocks, the deviant stimuli differed from the standards either in frequency (650 Hz), intensity (70 dB) or duration (20 msec). Left- and right-ear stimulations were used in separate blocks. Event-related brain potentials (ERPs) were recorded with 16 electrodes over both hemispheres. All the different types of deviant stimuli elicited an ERP component called the mismatch negativity (MMN). The MMN was larger over the right hemisphere irrespective of the ear stimulated whereas the N1 component, elicited by both standards and deviants, was larger over the hemisphere contralateral to the ear stimulated. The results provide further evidence for the view that the MMN reflects a neural mismatch process with a memory trace which automatically codes the physical features of the repetitive stimuli.

Attentional modulation of human auditory cortex

Attention powerfully influences auditory perception, but little is understood about the mechanisms whereby attention sharpens responses to unattended sounds. We used high-resolution surface mapping techniques (using functional magnetic resonance imaging, fMRI) to examine activity in human auditory cortex during an intermodal selective attention task. Stimulus-dependent activations (SDAs), evoked by unattended sounds during demanding visual tasks, were maximal over mesial auditory cortex. They were tuned to sound frequency and location, and showed rapid adaptation to repeated sounds. Attention-related modulations (ARMs) were isolated as response enhancements that occurred when subjects performed pitch-discrimination tasks. In contrast to SDAs, ARMs were localized to lateral auditory cortex, showed broad frequency and location tuning, and increased in amplitude with sound repetition. The results suggest a functional dichotomy of auditory cortical fields: stimulus-determined mesial fields that faithfully transmit acoustic information, and attentionally labile lateral fields that analyze acoustic features of behaviorally relevant sounds.