Hanna Renvall

Sound Categories Are Represented as Distributed Patterns in the Human Auditory Cortex

The ability to recognize sounds allows humans and animals to efficiently detect behaviorally relevant events, even in the absence of visual information. Sound recognition in the human brain has been assumed to proceed through several functionally specialized areas, culminating in cortical modules where category-specific processing is carried out. In the present high-resolution fMRI experiment, we challenged this model by using well-controlled natural auditory stimuli and by employing an advanced analysis strategy based on an iterative machine-learning algorithm that allows modeling of spatially distributed, as well as localized, response patterns. Sounds of cats, female singers, acoustic guitars, and tones were controlled for their time-varying spectral characteristics and presented to subjects at three different pitch levels. Sound category information--not detectable with conventional contrast-based methods analysis--could be detected with multivoxel pattern analyses and attributed to spatially distributed areas over the supratemporal cortices. A more localized pattern was observed for processing of pitch laterally to primary auditory areas. Our findings indicate that distributed neuronal populations within the human auditory cortices, including areas conventionally associated with lower-level auditory processing, entail categorical representations of sounds beyond their physical properties.

Functional Magnetic Resonance Imaging Blood Oxygenation Level-Dependent Signal and Magnetoencephalography Evoked Responses Yield Different Neural Functionality in Reading

It is often implicitly assumed that the neural activation patterns revealed by hemodynamic methods, such as functional magnetic resonance imaging (fMRI), and electrophysiological methods, such as magnetoencephalography (MEG) and electroencephalography (EEG), are comparable. In early sensory processing that seems to be the case, but the assumption may not be correct in high-level cognitive tasks. For example, MEG and fMRI literature of single-word reading suggests differences in cortical activation, but direct comparisons are lacking. Here, while the same human participants performed the same reading task, analysis of MEG evoked responses and fMRI blood oxygenation level-dependent (BOLD) signals revealed marked functional and spatial differences in several cortical areas outside the visual cortex. Divergent patterns of activation were observed in the frontal and temporal cortex, in accordance with previous separate MEG and fMRI studies of reading. Furthermore, opposite stimulus effects in the MEG and fMRI measures were detected in the left occipitotemporal cortex: MEG evoked responses were stronger to letter than symbol strings, whereas the fMRI BOLD signal was stronger to symbol than letter strings. The EEG recorded simultaneously during MEG and fMRI did not indicate neurophysiological differences that could explain the observed functional discrepancies between the MEG and fMRI results. Acknowledgment of the complementary nature of hemodynamic and electrophysiological measures, as reported here in a cognitive task using evoked response analysis in MEG and BOLD signal analysis in fMRI, represents an essential step toward an informed use of multimodal imaging that reaches beyond mere combination of location and timing of neural activation.

Attention modulates the auditory cortical processing of spatial and category cues in naturalistic auditory scenes

This combined fMRI and MEG study investigated brain activations during listening and attending to natural auditory scenes. We first recorded, using in-ear microphones, vocal non-speech sounds, and environmental sounds that were mixed to construct auditory scenes containing two concurrent sound streams. During the brain measurements, subjects attended to one of the streams while spatial acoustic information of the scene was either preserved (stereophonic sounds) or removed (monophonic sounds). Compared to monophonic sounds, stereophonic sounds evoked larger blood-oxygenation-level-dependent (BOLD) fMRI responses in the bilateral posterior superior temporal areas, independent of which stimulus attribute the subject was attending to. This finding is consistent with the functional role of these regions in the (automatic) processing of auditory spatial cues. Additionally, significant differences in the cortical activation patterns depending on the target of attention were observed. Bilateral planum temporale and inferior frontal gyrus were preferentially activated when attending to stereophonic environmental sounds, whereas when subjects attended to stereophonic voice sounds, the BOLD responses were larger at the bilateral middle superior temporal gyrus and sulcus, previously reported to show voice sensitivity. In contrast, the time-resolved MEG responses were stronger for mono- than stereophonic sounds in the bilateral auditory cortices at ~360 ms after the stimulus onset when attending to the voice excerpts within the combined sounds. The observed effects suggest that during the segregation of auditory objects from the auditory background, spatial sound cues together with other relevant temporal and spectral cues are processed in an attention-dependent manner at the cortical locations generally involved in sound recognition. More synchronous neuronal activation during monophonic than stereophonic sound processing, as well as (local) neuronal inhibitory mechanisms in the auditory cortex, may explain the simultaneous increase of BOLD responses and decrease of MEG responses. These findings highlight the complimentary role of electrophysiological and hemodynamic measures in addressing brain processing of complex stimuli.

Children show right-lateralized effects of spoken word-form learning

It is commonly thought that phonological learning is different in young children compared to adults, possibly due to the speech processing system not yet having reached full native-language specialization. However, the neurocognitive mechanisms of phonological learning in children are poorly understood. We employed magnetoencephalography (MEG) to track cortical correlates of incidental learning of meaningless word forms over two days as 6–8-year-olds overtly repeated them. Native (Finnish) pseudowords were compared with words of foreign sound structure (Korean) to investigate whether the cortical learning effects would be more dependent on previous proficiency in the language rather than maturational factors. Half of the items were encountered four times on the first day and once more on the following day. Incidental learning of these recurring word forms manifested as improved repetition accuracy and a correlated reduction of activation in the right superior temporal cortex, similarly for both languages and on both experimental days, and in contrast to a salient left-hemisphere emphasis previously reported in adults. We propose that children, when learning new word forms in either native or foreign language, are not yet constrained by left-hemispheric segmental processing and established sublexical native-language representations. Instead, they may rely more on supra-segmental contours and prosody.

Parametric Merging of MEG and fMRI Reveals Spatiotemporal Differences in Cortical Processing of Spoken Words and Environmental Sounds in Background Noise

There is an increasing interest to integrate electrophysiological and hemodynamic measures for characterizing spatial and temporal aspects of cortical processing. However, an informative combination of responses that have markedly different sensitivities to the underlying neural activity is not straightforward, especially in complex cognitive tasks. Here, we used parametric stimulus manipulation in magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) recordings on the same subjects, to study effects of noise on processing of spoken words and environmental sounds. The added noise influenced MEG response strengths in the bilateral supratemporal auditory cortex, at different times for the different stimulus types. Specifically for spoken words, the effect of noise on the electrophysiological response was remarkably nonlinear. Therefore, we used the single-subject MEG responses to construct parametrization for fMRI data analysis and obtained notably higher sensitivity than with conventional stimulus-based parametrization. fMRI results showed that partly different temporal areas were involved in noise-sensitive processing of words and environmental sounds. These results indicate that cortical processing of sounds in background noise is stimulus specific in both timing and location and provide a new functionally meaningful platform for combining information obtained with electrophysiological and hemodynamic measures of brain function.

Genome-Wide Linkage Analysis of Human Auditory Cortical Activation Suggests Distinct Loci on Chromosomes 2, 3, and 8

Neural processes are explored through macroscopic neuroimaging and microscopic molecular measures, but the two levels remain primarily detached. The identification of direct links between the levels would facilitate use of imaging signals as probes of genetic function and, vice versa, access to molecular correlates of imaging measures. Neuroimaging patterns have been mapped for a few isolated genes, chosen based on their connection with a clinical disorder. Here we propose an approach that allows an unrestricted discovery of the genetic basis of a neuroimaging phenotype in the normal human brain. The essential components are a subject population that is composed of relatives and selection of a neuroimaging phenotype that is reproducible within an individual and similar between relatives but markedly variable across a population. Our present combined magnetoencephalography and genome-wide linkage study in 212 healthy siblings demonstrates that auditory cortical activation strength is highly heritable and, specifically in the right hemisphere, regulated oligogenically with linkages to chromosomes 2q37, 3p12, and 8q24. The identified regions delimit as candidate genes TRAPPC9, operating in neuronal differentiation, and ROBO1, regulating projections of thalamocortical axons. Identification of normal genetic variation underlying neurophysiological phenotypes offers a non-invasive platform for an in-depth, concerted capitalization of molecular and neuroimaging levels in exploring neural function.

Distinct Effects of Memory Retrieval and Articulatory Preparation when Learning and Accessing New Word Forms

Temporal and frontal activations have been implicated in learning of novel word forms, but their specific roles remain poorly understood. The present magnetoencephalography (MEG) study examines the roles of these areas in processing newly-established word form representations. The cortical effects related to acquiring new phonological word forms during incidental learning were localized. Participants listened to and repeated back new word form stimuli that adhered to native phonology (Finnish pseudowords) or were foreign (Korean words), with a subset of the stimuli recurring four times. Subsequently, a modified 1-back task and a recognition task addressed whether the activations modulated by learning were related to planning for overt articulation, while parametrically added noise probed reliance on developing memory representations during effortful perception. Learning resulted in decreased left superior temporal and increased bilateral frontal premotor activation for familiar compared to new items. The left temporal learning effect persisted in all tasks and was strongest when stimuli were embedded in intermediate noise. In the noisy conditions, native phonotactics evoked overall enhanced left temporal activation. In contrast, the frontal learning effects were present only in conditions requiring overt repetition and were more pronounced for the foreign language. The results indicate a functional dissociation between temporal and frontal activations in learning new phonological word forms: the left superior temporal responses reflect activation of newly-established word-form representations, also during degraded sensory input, whereas the frontal premotor effects are related to planning for articulation and are not preserved in noise.

Evidence for genetic regulation of the human parieto-occipital 10-Hz rhythmic activity

Several functional and morphological brain measures are partly under genetic control. The identification of direct links between neuroimaging signals and corresponding genetic factors can reveal cellular‐level mechanisms behind the measured macroscopic signals and contribute to the use of imaging signals as probes of genetic function. To uncover possible genetic determinants of the most prominent brain signal oscillation, the parieto‐occipital 10‐Hz alpha rhythm, we measured spontaneous brain activity with magnetoencephalography in 210 healthy siblings while the subjects were resting, with eyes closed and open. The reactivity of the alpha rhythm was quantified from the difference spectra between the two conditions. We focused on three measures: peak frequency, peak amplitude and the width of the main spectral peak. In accordance with earlier electroencephalography studies, spectral peak amplitude was highly heritable (h2 > 0.75). Variance component‐based analysis of 28 000 single‐nucleotide polymorphism markers revealed linkage for both the width and the amplitude of the spectral peak. The strongest linkage was detected for the width of the spectral peak over the left parieto‐occipital cortex on chromosome 10 (LOD = 2.814, nominal P < 0.03). This genomic region contains several functionally plausible genes, including GRID1 and ATAD1 that regulate glutamate receptor channels mediating synaptic transmission, NRG3 with functions in brain development and HRT7 involved in the serotonergic system and circadian rhythm. Our data suggest that the alpha oscillation is in part genetically regulated, and that it may be possible to identify its regulators by genetic analyses on a realistically modest number of samples.

Slow wave oscillations in awake healthy subjects - methodological and physiological considerations

Purpose: Detection of pathologic slow-wave oscillations (0.5–7 Hz) in awake subjects has gained increasing interest in clinical diagnostics. Their significance, however, is hampered by the occasional presence of slow waves in healthy subjects, as well as the abundance of artefactual signals at low measurement frequencies. The aim of this study was to assess the occurrence of slow-wave oscillations in healthy subjects and to sharpen the management of possible measurement artifacts, in order to create a normative database for neurological patients. Methods: The authors analyzed magnetoencephalography recordings of spontaneous brain oscillations in 139 awake healthy adults. Sources of artifacts were first identified and suppressed by temporal extension of signal space separation method, and the remaining artifact components were projected out using signal space projection. Individual amplitude spectra were compared with the channel-level average spectra over all subjects. Results: Slow-wave oscillations deviating ±2 standard deviations from the average spectrum were detected in 12 subjects (∼9%). In 10 subjects, the oscillations were considered as normal physiological phenomena. Only two subjects showed activity that could have been interpreted as pathological: one subject with widespread parietal bilateral polyrhythmic slow-wave activity and one with focal rolandic 2.7-Hz slow-wave activity. Conclusions: The prevalence of slow-wave oscillations in a healthy adult population is low. Knowledge about their occurrence, however, is essential for interpreting their significance in brain diseases. Artifacts and benign oscillatory variants at slow frequencies have to be recognized.

Kernel Convolution Model for Decoding Sounds from Time-Varying Neural Responses

In this study we present a kernel based convolution model to characterize neural responses to natural sounds by decoding their time-varying acoustic features. The model allows to decode natural sounds from high-dimensional neural recordings, such as magneto encephalography (MEG), that track timing and location of human cortical signalling no invasively across multiple channels. We used the MEG responses recorded from subjects listening to acoustically different environmental sounds. By decoding the stimulus frequencies from the responses, our model was able to accurately distinguish between two different sounds that it had never encountered before with 70% accuracy. Convolution models typically decode frequencies that appear at a certain time point in the sound signal by using neural responses from that time point until a certain fixed duration of the response. Using our model, we evaluated several fixed durations (time-lags) of the neural responses and observed auditory MEG responses to be most sensitive to spectral content of the sounds at time-lags of 250 ms to 500 ms. The proposed model should be useful for determining what aspects of natural sounds are represented by high-dimensional neural responses and may reveal novel properties of neural signals.