Auditory Attention

Selective ATTENTION may be defined as a process by which the perception of certain stimuli in the environment is enhanced relative to other concurrent stimuli of lesser immediate priority. A classic auditory example of this phenomenon is the so-called cocktail party effect, wherein a person can selectively listen to one particular speaker while tuning out several other simultaneous conversations.

For many years, psychological theories of selective attention were traditionally divided between those advocating early levels of stimulus selection and those advocating late selection. Early selection theories held that there was an early filtering mechanism by which "channels" of irrelevant input could be attenuated or even rejected from further processing based on some simple physical attribute (BROADBENT 1970; Treisman 1969). In contrast, late selection theories held that all stimuli are processed to the same considerable detail, which generally meant through completion of perceptual analysis, before any selection due to attention took place (Deutsch and Deutsch 1963).

Various neurophysiological studies have attempted to shed light on both the validity of these theories and the neural mechanisms that underlie auditory attention. One possible neural mechanism for early stimulus selection would be the attenuation or gating of irrelevant input at the early levels of the sensory pathways by means of descending modulatory pathways (Hernandez-Peón, Scherrer, and Jouvet, 1956). For example, there is a descending pathway in the auditory system that parallels the ascending one all the way out to the cochlea (Brodal 1981), and direct electrical stimulation of this descending pathway at various levels, including auditory cortex, can inhibit the responses of the afferent auditory nerves to acoustic input. Other animal studies have indicated that stimulation of pathways from the frontal cortex and the mesencephalic reticular formation can modulate sensory transmission through the THALAMUS, thus providing another mechanism by which higher brain centers might modulate lower level processing during selective attention (Skinner and Yingling 1977). In addition, sensory processing activity in primary auditory CEREBRAL CORTEX or early auditory association cortices could conceivably be directly modulated by "descending" pathways from still higher cortical levels.

It has proven difficult, however, to demonstrate that any of these possible mechanisms for sensory modulation are actually used during auditory attention. Early animal studies purporting to show attenuation of irrelevant auditory input at the sensory periphery (Hernandez-Peón, Scherrer, and Jouvet 1956) were roundly criticized on methodological grounds (Worden 1966). Nevertheless, there have been animal studies providing evidence of some very early (i.e., brainstem-level) modulation of auditory processing as a function of attentional state or arousal (e.g., Oatman and Anderson 1977). In addition, Benson and Heinz (1978), studying single cells in monkey primary auditory cortex during a selective attention task (dichotic listening), reported relative enhancement of the responses to attended stimuli. Attending to sounds to perform sound localization vs. simple detection also has been shown to result in enhanced firing of units in auditory cortex (Benson, Heinz, and Goldstein 1981).

Auditory attention has been investigated extensively in humans using event- related potentials (ERPs) and event-related magnetic fields (ERFs). These recordings can noninvasively track with high temporal resolution the brain activity associated with different types of stimulus events. By analyzing changes in the ERPs or ERFs as a function of the direction of attention, one can make inferences about the timing, level of processing, and anatomical location of stimulus selection processes in the brain.

In an early seminal ERP study, Hillyard et al. (1973) implemented an experimental analog of the cocktail party effect and demonstrated differential processing of attended and unattended auditory stimuli at the level of the "N1" wave at ~100 msec poststimulus. More recent ERP studies furthering this approach have reported that focused auditory selective attention can affect stimulus processing as early as 20 msec poststimulus (the "P20-50" effect; Woldorff et al. 1987). Additional studies using ERPs (Woldorff and Hillyard 1991) and using ERFs and source-analysis modeling (Woldorff et al. 1993) indicated these electrophysiological attentional effects occurred in and around primary auditory cortex, had waveshapes that precisely took the form of an amplitude modulation of the early sensory-evoked components, and were colocalized with the sources of these sensory-evoked components. These results were interpreted as providing strong evidence for the existence of an attentionally modulated, sensory gain control of the auditory input channels at or before the initial stages of cortical processing, thereby providing strong support for early selection attentional theories that posit that stimulus input can be selected at levels considerably prior to the completion of perceptual analysis. Moreover, the very early onset latency of these attentional effects (20 ms) strongly suggests that this selection is probably accomplished by means of a top-down, preset biasing of the stimulus input channels.

On the other hand, reliable effects of attention on the earliest portion of the human auditory ERP reflecting auditory nerve and brainstem-level processing have generally not been found (Picton and Hillyard 1974), thus providing no evidence for peripheral filtering via the descending auditory pathway that terminates at the cochlea. Nevertheless, recent research measuring a different type of physiological response -- otoacoustic cochlear emissions -- has provided some evidence for such early filtering (Giard et al. 1991).

Additional evidence that attention can affect early auditory processing derives from studies of another ERP/ERF wave known as the mismatch negativity/mismatch field (MMN/MMF), which is elicited by deviant auditory stimuli in a series of identical stimuli. Because the MMN/MMF can be elicited in the absence of attention and by deviations in any of a number of auditory features, this wave was proposed to reflect a strong automaticity of the processing of auditory stimulus features (reviewed in Naatanen 1990 and 1992). Both the MMN (Woldorff et al. 1991) and the MMF (Woldorff et al. 1998), however, can also be modulated by attention, being greatly reduced when attention is strongly focused elsewhere, thus providing converging evidence that attention can influence early auditory sensory analysis. On the other hand, the elicitation of at least some MMN/MMF for many different feature deviations in a strongly ignored auditory channel has been interpreted as evidence that considerable feature analysis is still performed even for unattended auditory stimuli (Alho 1992). An intermediate view that may accommodate these findings is that various aspects of early auditory sensory processing and feature analysis may be "partially" or "weakly" automatic, occurring even in the absence of attention but still subject to top-down attentional modulation (Woldorff et al. 1991; Hackley 1993). Under this view, the very earliest stimulus processing (i.e., peripheral and brainstem levels) tends to be strongly automatic, but at the initial cortical levels there is a transition from strong to weak automaticity, wherein some amount of analysis is generally obligatory but is nevertheless modifiable by attention (reviewed in Hackley 1993).

There are also various slower-frequency, longer-latency ERP auditory attention effects that are not modulations of early sensory activity, but rather appear to reflect "endogenous," additional activations from both auditory and nonauditory association cortex (e.g., "processing negativity," target-related "N2b," "P300"). This type of activity occurs only or mainly for attended-channel stimuli or only for target stimuli within an attended channel and might reflect later selection, classification, or decision processes that also occur during auditory attention (reviewed in Alho 1992; Näätänen 1992). Attention to less discriminable features of auditory stimuli (Hansen and Hillyard 1983) or to a conjunction of auditory features (Woods et al. 1991) also produces longer-latency differential activation that may reflect later selection processes. In addition, there is a build-up of endogenous brain electrical activity (a "DC shift") as subjects begin to attend to a short stream of auditory stimuli (Hansen and Hillyard 1988), which could reflect some sort of initiation of the controlling executive function.

In contrast to electrophysiological studies, relatively few hemodynamically-based functional neuroimaging studies have been directed at studying auditory attention in humans. In a recent study using PO SITRON EMISSION TOMOGRAPHY (PET), O'Leary et al. (1996) reported enhanced activity in the auditory cortex contralateral to the direction of attention during a dichotic listening task. PET studies have also shown that attention to different aspects of speech sounds (e.g., phonetics vs. pitch) can affect the relative activation of the two hemispheres (Zatorre, Evans, and Meyer 1992). In addition, functional MAGNETIC RESONANCE IMAGING has indicated that intermodal attention can modulate auditory cortical processing (Woodruff et al. 1996).

Most neurophysiological studies of auditory attention in humans have focused on the effects of attention on the processing of sounds in auditory cortical areas. Less work has been directed toward elucidating the neural structures and mechanisms that control auditory attention. Based on various hemodynamic imaging studies, the anterior cingulate is likely to be involved, as it is activated during a number of cognitive and/or executive functions (Posner et al. 1988). In addition, human lesion studies suggest the prefrontal cortex is important for modulating the activity in the ipsilateral auditory cortex during auditory attention (Knight et al. 1981). It may be that some of the slower-frequency, endogenous ERP auditory attention effects reflect the activation of these areas as they serve to modulate or otherwise control auditory processing. Whether these mechanisms actually employ thalamic gating, some other modulatory mechanism, or a combination, is not yet known.

References

Alho, K. (1992). Selective attention in auditory processing as reflected in event-related brain potentials. Psychophysiology 29:247-263.

Benson, D. A., and R. D. Heinz. (1978). Single-unit activity in the auditory cortex of monkeys selectively attending left vs. right ear stimuli. Brain Research 159:307-320.

Benson, D. A., R. D. Heinz, and M. H. Goldstein, Jr. (1981). Single-unit activity in the auditory cortex actively localizing sound sources: spatial tuning and behavioral dependency. Brain Research 219:249-267.

Broadbent, D. E. (1970). Stimulus set and response set: Two kinds of selective attention. In D. I. Mostofsky, Ed., Attention: Contemporary Theory and Analysis. New York: Appleton-Century-Crofts, pp. 51-60.

Brodal, A. (1981). Neurological Anatomy. New York: Oxford University Press.

Deutsch, J. A., and D. Deutsch. (1963). Attention: some theoretical considerations. Psychological Review 70:80-90.

Giard, M. H., L. Collet, P. Bouchet, and J. Pernier. (1994). Auditory selective attention in the human cochlea. Brain Research 633:353-356.

Hackley, S. A. (1993). An evaluation of the automaticity of sensory processing using event-related potentials and brain-stem reflexes. Psychophysiology 30:415-428.

Hansen, J. C., and S. A. Hillyard. (1983). Selective attention to multidimensional auditory stimuli. J. of Exp. Psychology: Human Perc. and Perf 9:1-18.

Hansen, J. C., and S. A. Hillyard. (1988). Temporal dynamics of human auditory selective attention. Psychophysiology 25:316-329.

Hernandez-Peón, R., H. Scherrer, and M. Jouvet. (1956). Modification of electrical activity in the cochlear nucleus during attention in unanesthetized cats. Science 123:331-332.

Hillyard, S. A., R. F. Hink, V. L. Schwent, and T. W. Picton. (1973). Electrical signs of selective attention in the human brain. Science 182:177-179.

Knight, R. T., S. A. Hillyard, D. L. Woods, and H. J. Neville. (1981). The effects of frontal cortex lesions on event-related potentials during auditory selective attention. Electroenceph. Clin. Neurophysiol. 52:571-582.

Naatanen, R. (1990). The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behavior and Brain Science 13:201-288.

Naatanen, R. (1992). Attention and Brain Function. Hillsdale, NJ: Erlbaum.

Oatman, L. C., and B. W. Anderson. (1977). Effects of visual attention on tone-burst evoked auditory potentials. Experimental Neurology 57:200-211.

O'Leary, D. S., N. C. Andreasen, R. R. Hurtig, R. D. Hichwa, G. L. Watkins, L. L. B. Ponto, M. Rogers, and P. T. Kirchner. (1996). A positron emission tomography study of binaurally- and dichotically-presented stimuli: Effects of level of language and directed attention. Brain and Language 53:20-39.

Picton, T. W., and S. A. Hillyard. (1974). Human auditory evoked potentials: II. Effects of attention. Electroenceph. Clin. Neurophysiol 36:191-199.

Posner, M. I., S. E. Petersen, P. T. Fox, and M. E. Raichle. (1988). Localization of cognitive operations in the human brain. Science 240:1627-1631.

Skinner, J. E., and C. D. Yingling. (1977). Central gating mechanisms that regulate event-related potentials and behavior. In J. E. Desmedt, Ed., Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, vol. 1. New York: S. Karger, pp. 30-69.

Treisman, A. (1969). Stategies and models of selective attention. Psych. Review 76:282-299.

Woldorff, M. G., C. C. Gallen, S. A. Hampson, S. A. Hillyard, C. Pantev, D. Sobel, and F. E. Bloom. (1993). Modulation of early sensory processing in human auditory cortex during auditory selective attention. Proc. Natl. Acad. Sci. 90:8722-8726.

Woldorff, M., S. A. Hackley, and S. A. Hillyard. (1991). The effects of channel-selective attention on the mismatch negativity wave elicited by deviant tones. Psychophysiology 28:30-42.

Woldorff M., J. C. Hansen, and S. A. Hillyard. (1987). Evidence for effects of selective attention in the mid-latency range of the human auditory event-related potential. In R. Johnson, Jr., R. Parasuraman, and J. W. Rohrbaugh, Eds., Current Trends in Event-Related Potential Research (EEGJ Suppl. 40). Amsterdam: Elsevier, pp. 146-54.

Woldorff, M. G., and S. A. Hillyard. (1991). Modulation of early auditory processing during selective listening to rapidly presented tones. Electroenceph. and Clin. Neurophysiology 79:170-191.

Woldorff, M. G., S. A. Hillyard, C. C. Gallen, S. A. Hampson, and F. E. Bloom. (1998). Magnetoencephalographic recordings demonstrate attentional modulation of mismatch-related neural activity in human auditory cortex. Psychophysiology 35:283-292.

Woodruff, P. W., R. R. Benson, P. A. Bandetinni, K. K. Kwong, R. J. Howard, T. Talavage, J. Belliveua, and B. R. Rosen. (1996). Modulation of auditory and visual cortex by selective attention is modality-dependent. Neuroreport 7:1909-1913.

Woods, D. L., K. Alho, and A. Algazi. (1991). Brain potential signs of feature processing during auditory selective attention. Neuroreport 2:189-192.

Worden, F. G. (1966). Attention and auditory electrophysiology. In F. Stellar and J. M. Sprague, Eds., Progress in Physiological Psychology. New York: Academic Press, pp. 45-116.

Zatorre, R. J., A. C. Evans, and E. Meyer. (1992). Lateralization of phonetic and pitch discrimination in speech processing. Science 256:846-849.

Auditory Attention

See also

References

Further Readings