Elsevier

Brain Research

Volume 812, Issues 1–2, 23 November 1998, Pages 23-37
Brain Research

Research report
A distributed cortical network for auditory sensory memory in humans

https://doi.org/10.1016/S0006-8993(98)00851-8Get rights and content

Abstract

Auditory sensory memory is a critical first stage in auditory perception that permits listeners to integrate incoming acoustic information with stored representations of preceding auditory events. Here, we investigated the neural circuits of sensory memory using behavioral and electrophysiological measures of auditory processing in patients with unilateral brain damage to dorsolateral prefrontal cortex, posterior association cortex, or the hippocampus. We used a neurophysiological marker of an automatic component of sensory memory, the mismatch negativity (MMN), which can be recorded without overt attention. In comparison with control subjects, temporal-parietal patients had impaired auditory discrimination and reduced MMN amplitudes with both effects evident only following stimuli presented in the ear contralateral to the lesioned hemisphere. This suggests that auditory sensory memories are predominantly stored in auditory cortex contralateral to the ear of presentation. Dorsolateral prefrontal damage impaired performance and reduced MMNs elicited by deviant stimuli presented in either ear, implying that dorsolateral prefrontal cortices have a bilateral facilitatory effect on sensory memory storage. Hippocampal lesions did not affect either performance or electrophysiological measures. The results provide evidence of a temporal-prefrontal neocortical network critical for the transient storage of auditory stimuli.

Introduction

Behavioral studies 6, 13, 14, 35have established that human short term memory is not a unitary phenomenon but rather an ensemble of components that includes sensory and working memory. Sensory memory refers to the automatic, transient storage of the sensory features of incoming stimuli for subsequent integration with previously presented stimuli and/or recalled information. This memory is particularly important in audition because the perception of speech and music requires integration of successive stimulus features that occur over short intervals. An important distinction between sensory and working memory is that the latter involves effortful, attentional controlled processing whereas the former is more automatic.

The representation of sounds in sensory memory lasts for several seconds 13, 14, 33and is thought to involve a complex and widely distributed neural network including both cortical and subcortical components. Lesion studies in human 7, 11, 51, 62and nonhuman primates 12, 22, 54show impaired auditory discrimination following damage to auditory cortex, suggesting that short-term memory involves the activation of modality-specific association cortex. Single-cell recordings in primates 8, 16, 20, along with neuropsychological 11, 62, and neuroimaging [61]studies in humans have suggested that the dorsolateral prefrontal cortex plays a critical role in a variety of short-term memory processes, possibly including sensory memory. The hippocampus is essential for normal long-term memory storage [53], but its contribution to initial sensory encoding remains uncertain. Some studies report no significant effects of hippocampal damage 53, 55while others find impaired performance in delayed auditory recognition tasks [11]and reduced brain responses to novel, or surprising events [25].

In the current study, the neural substrates of auditory sensory memory were investigated by recording event-related brain potentials (ERPs) in patients with focal brain damage either to the temporal-parietal cortex, the dorsolateral prefrontal cortex, or the medial temporal lobe including hippocampal and parahippocampal gyri (see Fig. 1). We examined the effect of these focal brain lesions on a neurophysiological index of sensory memory, the mismatch negativity (MMN), and on auditory discrimination. The MMN is particularly well-suited for studying the neural correlates of sensory memory because it is elicited in paradigms in which overt attention and behavioral responses are not required (e.g., when participants read a book). Abnormalities of initial sensory memory would be predicted to produce corresponding deficits in auditory discrimination performance.

The MMN is elicited by deviant stimuli embedded in sequences of standard stimuli. The deviant sounds may differ from the standard sounds in such dimensions as frequency, duration, intensity, spatial location, or spectral patterns 29, 37, 38. Deviations from simple auditory patterns, such as occasional repetitions occurring in a sequence of tones that otherwise alternate regularly in frequency, also generate an MMN 2, 3, 41. MMN generation depends on the ability to maintain a memory of the types of stimuli presented 37, 49, 56and, thus, provides a direct and noninvasive measure of auditory sensory memory in the human brain 37, 49, 56. For instance, deviant stimuli presented alone do not generate an MMN [39]and backward masking reduces MMN amplitudes in a manner that corresponds to performance decrements 56, 57. In his influential review, Näätänen has suggested that the MMN reflects a neural mismatch between an incoming stimulus and the transient representation of sounds in short-term memory [37].

The neural network underlying MMN generation has attracted considerable attention over the last decade. Scalp topography analysis [18], neuromagnetic recording 21, 31, dipole source modeling [50]and animal models 15, 23suggest that the MMN reflects activity from neuronal ensembles in or near the primary auditory cortices. Evidence from scalp current source density mapping and dipole source modeling suggest possible additional sources in prefrontal [18]and parietal cortex [31]. Although it is often assumed that the MMN reflects a distributed network involving auditory cortex, prefrontal cortex and parietal cortex, few lesion studies have addressed this issue 1, 4. However, source analysis of human ERPs and lesion studies of nonhuman primates imply that dorsolateral prefrontal and temporal-parietal lesions might be expected to impair auditory discrimination and concurrently reduce MMN amplitudes.

Section snippets

Participants

Participants were patients with focal brain lesions following a stroke in either the temporal-parietal cortex, the dorsolateral prefrontal cortex, or medial temporal cortex. Temporal-parietal lesions included the lateral superior temporal gyrus, the posterior superior temporal plane including Heschls gyri and Brodmann area 22, the superior temporal sulcus and inferior parietal areas 39 and 40 (Fig. 1A). Lesions were due to infarction of the posterior temporal branch of the middle cerebral

Results

In the analyses of the behavioral and ERP data the effect of deviant type did not interact with the effect of lesions so the data were collapsed across this variable.

Discussion

The N1 deflection is thought to receive contribution from a distributed neural network that includes generators located in the temporal lobes with possible additional sources in the frontal lobe (Ref. 17, 45, for a review see Refs. 40, 58). The contribution of the temporal-parietal cortex in the generation of the N1 wave is supported by intracerebral recording in humans 32, 48, lesion studies 26, 28, 60and dipole source modeling studies 45, 50. In the current study, temporal-parietal lesions

Acknowledgements

This study was supported by an FRSQ postdoctoral fellowship to the first author and by NINDS grant NS32893 to the second author and NINDS grants NS21135 and NS17778 to the third author.

References (62)

  • R.T. Knight et al.

    The effects of lesions of superior temporal gyrus and inferior parietal lobe on temporal and vertex components of the human AEP

    Electroencephalogr. Clin. Neurophysiol.

    (1988)
  • C. Liegeois-Chauvel et al.

    Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components

    Electroencephalogr. Clin. Neurophysiol.

    (1994)
  • R. Näätänen et al.

    Do event-related potentials reveal the mechanism of the auditory sensory memory in the human brain

    Neurosci. Lett.

    (1989)
  • F. Richer et al.

    Intracerebral amplitude distributions of the auditory evoked potential

    Electroencephalogr. Clin. Neurophysiol.

    (1989)
  • W. Wickelgren

    Sparing of short-term memory in an amnesic patient: implications for strength theory of memory

    Neuropsychologia

    (1968)
  • I. Winkler et al.

    Event-related potentials in auditory backward recognition masking: a new way to study the neurophysiological basis of sensory memory in humans

    Neurosci. Lett.

    (1992)
  • D.L. Woods et al.

    Click spatial position influences middle latency auditory evoked potentials (MAEPs) in human

    Electroencephalogr. Clin. Neurophysiol.

    (1985)
  • D.L. Woods et al.

    Generators of middle and long-latency auditory evoked potentials: implications from studies of patients with bitemporal lesions

    Electroencephalogr. Clin. Neurophysiol.

    (1987)
  • C. Alain et al.

    Attention modulates auditory pattern memory as indexed by event-related brain potentials

    Psychophysiology

    (1997)
  • C. Alain et al.

    Brain indices of automatic pattern processing

    Neuroreport

    (1994)
  • A. Baddeley, Human Memory: Theory and Practice, Allyn and Bacon, Needham Height,...
  • U. Blaettner et al.

    Diagnosis of unilateral telencephalic hearing disorders

    Brain

    (1989)
  • M. Bodner et al.

    Auditory memory cells in dorsolateral prefrontal cortex

    Neuroreport

    (1996)
  • C. Cavada et al.

    Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticortical connections

    J. Comp. Neurol.

    (1989)
  • C. Cavada et al.

    Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticortical networks linking sensory and limbic areas with the frontal lobe

    J. Comp. Neurol.

    (1989)
  • L.L. Chao et al.

    Human prefrontal lesions increase distractibility to irrelevant sensory inputs

    Neuroreport

    (1995)
  • M. Colombo et al.

    Auditory association cortex lesions impair auditory short-term memory in monkey

    Science

    (1990)
  • N. Cowan

    On short and long auditory stores

    Psychol. Bull.

    (1984)
  • N. Cowan, Attention and Memory: an Integrated Framework, Oxford Univ. Press, New York,...
  • J.M. Fuster

    Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory

    J. Neurophysiol.

    (1973)
  • M.-H. Giard et al.

    Brain generators implicated in processing of auditory stimulus deviance: a topographic event-related potential study

    Psychophysiology

    (1990)
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