Timothy J. Herron

Functional Maps of Human Auditory Cortex: Effects of Acoustic Features and Attention

Background While human auditory cortex is known to contain tonotopically organized auditory cortical fields (ACFs), little is known about how processing in these fields is modulated by other acoustic features or by attention. Methodology/Principal Findings We used functional magnetic resonance imaging (fMRI) and population-based cortical surface analysis to characterize the tonotopic organization of human auditory cortex and analyze the influence of tone intensity, ear of delivery, scanner background noise, and intermodal selective attention on auditory cortex activations. Medial auditory cortex surrounding Heschls gyrus showed large sensory (unattended) activations with two mirror-symmetric tonotopic fields similar to those observed in non-human primates. Sensory responses in medial regions had symmetrical distributions with respect to the left and right hemispheres, were enlarged for tones of increased intensity, and were enhanced when sparse image acquisition reduced scanner acoustic noise. Spatial distribution analysis suggested that changes in tone intensity shifted activation within isofrequency bands. Activations to monaural tones were enhanced over the hemisphere contralateral to stimulation, where they produced activations similar to those produced by binaural sounds. Lateral regions of auditory cortex showed small sensory responses that were larger in the right than left hemisphere, lacked tonotopic organization, and were uninfluenced by acoustic parameters. Sensory responses in both medial and lateral auditory cortex decreased in magnitude throughout stimulus blocks. Attention-related modulations (ARMs) were larger in lateral than medial regions of auditory cortex and appeared to arise primarily in belt and parabelt auditory fields. ARMs lacked tonotopic organization, were unaffected by acoustic parameters, and had distributions that were distinct from those of sensory responses. Unlike the gradual adaptation seen for sensory responses, ARMs increased in amplitude throughout stimulus blocks. Conclusions/Significance The results are consistent with the view that medial regions of human auditory cortex contain tonotopically organized core and belt fields that map the basic acoustic features of sounds while surrounding higher-order parabelt regions are tuned to more abstract stimulus attributes. Intermodal selective attention enhances processing in neuronal populations that are partially distinct from those activated by unattended stimuli.

Functional Properties of Human Auditory Cortical Fields

While auditory cortex in non-human primates has been subdivided into multiple functionally specialized auditory cortical fields (ACFs), the boundaries and functional specialization of human ACFs have not been defined. In the current study, we evaluated whether a widely accepted primate model of auditory cortex could explain regional tuning properties of fMRI activations on the cortical surface to attended and non-attended tones of different frequency, location, and intensity. The limits of auditory cortex were defined by voxels that showed significant activations to non-attended sounds. Three centrally located fields with mirror-symmetric tonotopic organization were identified and assigned to the three core fields of the primate model while surrounding activations were assigned to belt fields following procedures similar to those used in macaque fMRI studies. The functional properties of core, medial belt, and lateral belt field groups were then analyzed. Field groups were distinguished by tonotopic organization, frequency selectivity, intensity sensitivity, contralaterality, binaural enhancement, attentional modulation, and hemispheric asymmetry. In general, core fields showed greater sensitivity to sound properties than did belt fields, while belt fields showed greater attentional modulation than core fields. Significant distinctions in intensity sensitivity and contralaterality were seen between adjacent core fields A1 and R, while multiple differences in tuning properties were evident at boundaries between adjacent core and belt fields. The reliable differences in functional properties between fields and field groups suggest that the basic primate pattern of auditory cortex organization is preserved in humans. A comparison of the sizes of functionally defined ACFs in humans and macaques reveals a significant relative expansion in human lateral belt fields implicated in the processing of speech.

Auditory Attention Activates Peripheral Visual Cortex

Background Recent neuroimaging studies have revealed that putatively unimodal regions of visual cortex can be activated during auditory tasks in sighted as well as in blind subjects. However, the task determinants and functional significance of auditory occipital activations (AOAs) remains unclear. Methodology/Principal Findings We examined AOAs in an intermodal selective attention task to distinguish whether they were stimulus-bound or recruited by higher-level cognitive operations associated with auditory attention. Cortical surface mapping showed that auditory occipital activations were localized to retinotopic visual cortex subserving the far peripheral visual field. AOAs depended strictly on the sustained engagement of auditory attention and were enhanced in more difficult listening conditions. In contrast, unattended sounds produced no AOAs regardless of their intensity, spatial location, or frequency. Conclusions/Significance Auditory attention, but not passive exposure to sounds, routinely activated peripheral regions of visual cortex when subjects attended to sound sources outside the visual field. Functional connections between auditory cortex and visual cortex subserving the peripheral visual field appear to underlie the generation of AOAs, which may reflect the priming of visual regions to process soon-to-appear objects associated with unseen sound sources.

Improving digit span assessment of short-term verbal memory

We measured digit span (DS) in two experiments that used computerized presentation of randomized auditory digits with performance-adapted list length adjustment. A new mean span (MS) metric of DS was developed that showed reduced variance, improved test–retest reliability, and higher correlations with the results of other neuropsychological test results when compared to traditional DS measures. The MS metric also enhanced the sensitivity of forward versus backward span comparisons, enabled the development of normative performance criteria with subdigit precision, and elucidated changes in DS performance with age and education level. Computerized stimulus delivery and improved scoring metrics significantly enhance the precision of DS assessments of short-term verbal memory.

Perceptual training improves syllable identification in new and experienced hearing aid users

We assessed the effects of perceptual training of syllable identification in noise on nonsense syllable test (NST) performance of new (Experiment 1) and experienced (Experiment 2) hearing aid (HA) users with sensorineural hearing loss. In Experiment 1, new HA users were randomly assigned to either immediate training (IT) or delayed training (DT) groups. IT subjects underwent 8 weeks of at-home syllable identification training and in-laboratory testing, whereas DT subjects underwent identical in-laboratory testing without training. Training produced large improvements in syllable identification in IT subjects, whereas spontaneous improvement was minimal in DT subjects. DT subjects then underwent training and showed performance improvements comparable with those of the IT group. Training-related improvement in NST scores significantly exceeded improvements due to amplification. In Experiment 2, experienced HA users received identical training and testing procedures as users in Experiment 1. The experienced users also showed significant training benefit. Training-related improvements generalized to untrained voices and were maintained on retention tests. Perceptual training appears to be a promising tool for improving speech perception in new and experienced HA users.

Stimulus-dependent activations and attention-related modulations in the auditory cortex: A meta-analysis of fMRI studies

We meta-analyzed 115 functional magnetic resonance imaging (fMRI) studies reporting auditory-cortex (AC) coordinates for activations related to active and passive processing of pitch and spatial location of non-speech sounds, as well as to the active and passive speech and voice processing. We aimed at revealing any systematic differences between AC surface locations of these activations by statistically analyzing the activation loci using the open-source Matlab toolbox VAMCA (Visualization and Meta-analysis on Cortical Anatomy). AC activations associated with pitch processing (e.g., active or passive listening to tones with a varying vs. fixed pitch) had median loci in the middle superior temporal gyrus (STG), lateral to Heschls gyrus. However, median loci of activations due to the processing of infrequent pitch changes in a tone stream were centered in the STG or planum temporale (PT), significantly posterior to the median loci for other types of pitch processing. Median loci of attention-related modulations due to focused attention to pitch (e.g., attending selectively to low or high tones delivered in concurrent sequences) were, in turn, centered in the STG or superior temporal sulcus (STS), posterior to median loci for passive pitch processing. Activations due to spatial processing were centered in the posterior STG or PT, significantly posterior to pitch processing loci (processing of infrequent pitch changes excluded). In the right-hemisphere AC, the median locus of spatial attention-related modulations was in the STS, significantly inferior to the median locus for passive spatial processing. Activations associated with speech processing and those associated with voice processing had indistinguishable median loci at the border of mid-STG and mid-STS. Median loci of attention-related modulations due to attention to speech were in the same mid-STG/STS region. Thus, while attention to the pitch or location of non-speech sounds seems to recruit AC areas less involved in passive pitch or location processing, focused attention to speech predominantly enhances activations in regions that already respond to human vocalizations during passive listening. This suggests that distinct attention mechanisms might be engaged by attention to speech and attention to more elemental auditory features such as tone pitch or location. This article is part of a Special Issue entitled Human Auditory Neuroimaging.

Factors influencing the latency of simple reaction time

Simple reaction time (SRT), the minimal time needed to respond to a stimulus, is a basic measure of processing speed. SRTs were first measured by Francis Galton in the 19th century, who reported visual SRT latencies below 190 ms in young subjects. However, recent large-scale studies have reported substantially increased SRT latencies that differ markedly in different laboratories, in part due to timing delays introduced by the computer hardware and software used for SRT measurement. We developed a calibrated and temporally precise SRT test to analyze the factors that influence SRT latencies in a paradigm where visual stimuli were presented to the left or right hemifield at varying stimulus onset asynchronies (SOAs). Experiment 1 examined a community sample of 1469 subjects ranging in age from 18 to 65. Mean SRT latencies were short (231, 213 ms when corrected for hardware delays) and increased significantly with age (0.55 ms/year), but were unaffected by sex or education. As in previous studies, SRTs were prolonged at shorter SOAs and were slightly faster for stimuli presented in the visual field contralateral to the responding hand. Stimulus detection time (SDT) was estimated by subtracting movement initiation time, measured in a speeded finger tapping test, from SRTs. SDT latencies averaged 131 ms and were unaffected by age. Experiment 2 tested 189 subjects ranging in age from 18 to 82 years in a different laboratory using a larger range of SOAs. Both SRTs and SDTs were slightly prolonged (by 7 ms). SRT latencies increased with age while SDT latencies remained stable. Precise computer-based measurements of SRT latencies show that processing speed is as fast in contemporary populations as in the Victorian era, and that age-related increases in SRT latencies are due primarily to slowed motor output.

Multimodal surface-based morphometry reveals diffuse cortical atrophy in traumatic brain injury.

BackgroundPatients with traumatic brain injury (TBI) often present with significant cognitive deficits without corresponding evidence of cortical damage on neuroradiological examinations. One explanation for this puzzling observation is that the diffuse cortical abnormalities that characterize TBI are difficult to detect with standard imaging procedures. Here we investigated a patient with severe TBI-related cognitive impairments whose scan was interpreted as normal by a board-certified radiologist in order to determine if quantitative neuroimaging could detect cortical abnormalities not evident with standard neuroimaging procedures.MethodsCortical abnormalities were quantified using multimodal surfaced-based morphometry (MSBM) that statistically combined information from high-resolution structural MRI and diffusion tensor imaging (DTI). Normal values of cortical anatomy and cortical and pericortical DTI properties were quantified in a population of 43 healthy control subjects. Corresponding measures from the patient were obtained in two independent imaging sessions. These data were quantified using both the average values for each lobe and the measurements from each point on the cortical surface. The results were statistically analyzed as z-scores from the mean with a p < 0.05 criterion, corrected for multiple comparisons. False positive rates were verified by comparing the data from each control subject with the data from the remaining control population using identical statistical procedures.ResultsThe TBI patient showed significant regional abnormalities in cortical thickness, gray matter diffusivity and pericortical white matter integrity that replicated across imaging sessions. Consistent with the patients impaired performance on neuropsychological tests of executive function, cortical abnormalities were most pronounced in the frontal lobes.ConclusionsMSBM is a promising tool for detecting subtle cortical abnormalities with high sensitivity and selectivity. MSBM may be particularly useful in evaluating cortical structure in TBI and other neurological conditions that produce diffuse abnormalities in both cortical structure and tissue properties.

Regional variation, hemispheric asymmetries and gender differences in pericortical white matter.

Brain white matter tissue composition can be quantified using Diffusion Tensor Imaging (DTI) and Magnetization Transfer Imaging (MTI). Fractional Anisotropy (FA), derived from DTI, indexes the integrity, density and organization of axons. Magnetization Transfer Ratio (MTR), derived from MTI, indexes to the presence of cell membranes and myelin. The combined use of FA and MTR provides a more complete picture of white matter structure than either imaging modality in isolation. Here we describe the regional distribution of FA and MTR measurements of pericortical white matter in 56 young, healthy right-handed subjects. Significant regional and lobar differences are seen for both measures along with a significant gender difference in FA. Highly consistent hemispheric asymmetries in FA and MTR were observed, suggesting that the greater fiber coherence and increased myelination of fibers in left hemisphere perisylvian regions may provide a structural basis for left-hemisphere language dominance.

Automated measurement of the human corpus callosum using MRI

The corpus callosum includes the majority of fibers that connect the two cortical hemispheres. Studies of cross-sectional callosal morphometry and area have revealed developmental, gender, and hemispheric differences in healthy populations and callosal deficits associated with neurodegenerative disease and brain injury. However, accurate quantification of the callosum using magnetic resonance imaging is complicated by intersubject variability in callosal size, shape, and location and often requires manual outlining of the callosum in order to achieve adequate performance. Here we describe an objective, fully automated protocol that utilizes voxel-based images to quantify the area and thickness both of the entire callosum and of different callosal compartments. We verify the methods accuracy, reliability, robustness, and multisite consistency and make comparisons with manual measurements using public brain-image databases. An analysis of age-related changes in the callosum showed increases in length and reductions in thickness and area with age. A comparison of older subjects with and without mild dementia revealed that reductions in anterior callosal area independently predicted poorer cognitive performance after factoring out Mini-Mental Status Examination scores and normalized whole brain volume. Open-source software implementing the algorithm is available at www.nitrc.org/projects/c8c8.