What underlies the emergence of stimulus- and domain-specific neural responses? Commentary on Hernandez, Claussenius-Kalman, Ronderos, Castilla-Earls, Sun, Weiss, & Young (2018)

Hernandez et al (2018) provide a welcome historical perspective and synthesis of emergentist theories over the last decades, particularly in their focus on theoretical differences. Here we discuss a number of neuroimaging findings on the character and drivers of seemingly domain-selective neural response preferences, and how these might bear on the predictiveness of different emergentist accounts

Convergent and divergent fMRI responses in children and adults to increasing language production demands

In adults, patterns of neural activation associated with perhaps the most basic language skill—overt object naming—are extensively modulated by the psycholinguistic and visual complexity of the stimuli. Do children's brains react similarly when confronted with increasing processing demands, or they solve this problem in a different way? Here we scanned 37 children aged 7–13 and 19 young adults who performed a well-normed picture-naming task with 3 levels of difficulty. While neural organization for naming was largely similar in childhood and adulthood, adults had greater activation in all naming conditions over inferior temporal gyri and superior temporal gyri/supramarginal gyri. Manipulating naming complexity affected adults and children quite differently: neural activation, especially over the dorsolateral prefrontal cortex, showed complexity-dependent increases in adults, but complexity-dependent decreases in children. These represent fundamentally different responses to the linguistic and conceptual challenges of a simple naming task that makes no demands on literacy or metalinguistics. We discuss how these neural differences might result from different cognitive strategies used by adults and children during lexical retrieval/production as well as developmental changes in brain structure and functional connectivity

Audio-visual speech perception: a developmental ERP investigation

Being able to see a talking face confers a considerable advantage for speech perception in adulthood. However, behavioural data currently suggest that children fail to make full use of these available visual speech cues until age 8 or 9. This is particularly surprising given the potential utility of multiple informational cues during language learning. We therefore explored this at the neural level. The event-related potential (ERP) technique has been used to assess the mechanisms of audio-visual speech perception in adults, with visual cues reliably modulating auditory ERP responses to speech. Previous work has shown congruence-dependent shortening of auditory N1/P2 latency and congruence-independent attenuation of amplitude in the presence of auditory and visual speech signals, compared to auditory alone. The aim of this study was to chart the development of these well-established modulatory effects over mid-to-late childhood. Experiment 1 employed an adult sample to validate a child-friendly stimulus set and paradigm by replicating previously observed effects of N1/P2 amplitude and latency modulation by visual speech cues; it also revealed greater attenuation of component amplitude given incongruent audio-visual stimuli, pointing to a new interpretation of the amplitude modulation effect. Experiment 2 used the same paradigm to map cross-sectional developmental change in these ERP responses between 6 and 11 years of age. The effect of amplitude modulation by visual cues emerged over development, while the effect of latency modulation was stable over the child sample. These data suggest that auditory ERP modulation by visual speech represents separable underlying cognitive processes, some of which show earlier maturation than others over the course of development

In vivo functional and myeloarchitectonic mapping of human primary auditory areas

In contrast to vision, where retinotopic mapping alone can define areal borders, primary auditory areas such as A1 are best delineated by combining in vivo tonotopic mapping with postmortem cyto- or myeloarchitectonics from the same individual. We combined high-resolution (800 μm) quantitative T(1) mapping with phase-encoded tonotopic methods to map primary auditory areas (A1 and R) within the "auditory core" of human volunteers. We first quantitatively characterize the highly myelinated auditory core in terms of shape, area, cortical depth profile, and position, with our data showing considerable correspondence to postmortem myeloarchitectonic studies, both in cross-participant averages and in individuals. The core region contains two "mirror-image" tonotopic maps oriented along the same axis as observed in macaque and owl monkey. We suggest that these two maps within the core are the human analogs of primate auditory areas A1 and R. The core occupies a much smaller portion of tonotopically organized cortex on the superior temporal plane and gyrus than is generally supposed. The multimodal approach to defining the auditory core will facilitate investigations of structure-function relationships, comparative neuroanatomical studies, and promises new biomarkers for diagnosis and clinical studies

Extensive Tonotopic Mapping across Auditory Cortex Is recapitulated by spectrally directed attention and systematically related to Cortical Myeloarchitecture

Auditory selective attention is vital in natural soundscapes. But, it is unclear how attentional focus on the primary dimension of auditory representation - acoustic frequency - might modulate basic auditory functional topography during active listening. In contrast to visual selective attention, which is supported by motor-mediated optimization of input across saccades and pupil dilation, the primate auditory system has fewer means of differentially sampling the world. This makes spectrally-directed endogenous attention a particularly crucial aspect of auditory attention. Using a novel functional paradigm combined with quantitative MRI, we establish in male and female listeners that human frequency-band-selective attention drives activation in both myeloarchitectonically-estimated auditory core, and across the majority of tonotopically-mapped non-primary auditory cortex. The attentionally-driven best-frequency maps show strong concordance with sensory-driven maps in the same subjects across much of the temporal plane, with poor concordance in areas outside traditional auditory cortex. There is significantly greater activation across most of auditory cortex when best frequency is attended, versus ignored; the same regions do not show this enhancement when attending to the least-preferred frequency band. Finally, the results demonstrate that there is spatial correspondence between the degree of myelination and the strength of the tonotopic signal across a number of regions in auditory cortex. Strong frequency preferences across tonotopically-mapped auditory cortex spatially correlate with R1-estimated myeloarchitecture, indicating shared functional and anatomical organization that may underlie intrinsic auditory regionalization

A bilingual advantage in controlling language interference during sentence comprehension

This study compared the comprehension of syntactically simple with more complex sentences in Italian–English adult bilinguals and monolingual controls in the presence or absence of sentence-level interference. The task was to identify the agent of the sentence and we primarily examined the accuracy of response. The target sentence was signalled by the gender of the speaker, either a male or a female, and this varied over trials, where the target was spoken in a male voice the distractor was spoken in a female voice and vice versa. In contrast to other work showing a bilingual disadvantage in sentence comprehension under conditions of noise, we show that in this task, where voice permits selection of the target, adult bilingual speakers are in fact better able than their monolingual Italian peers to resist sentence-level interference when comprehension demands are high. Within bilingual speakers we also found that degree of proficiency in English correlated with the ability to resist interference for complex sentences both when the target and distractor were in Italian and when the target was in English and the distractor in Italian

Speech-in-speech perception, non-verbal selective attention, and musical training

Speech is more difficult to understand when it is presented concurrently with a distractor speech stream. One source of this difficulty is that competing speech can act as an attentional lure, requiring listeners to exert attentional control to ensure that attention does not drift away from the target. Stronger attentional control may enable listeners to more successfully ignore distracting speech, and so individual differences in selective attention may be one factor driving the ability to perceive speech in complex environments. However, the lack of a paradigm for measuring non-verbal sustained selective attention to sound has made this hypothesis difficult to test. Here we find that individuals who are better able to attend to a stream of tones and respond to occasional repeated sequences while ignoring a distractor tone stream are also better able to perceive speech masked by a single distractor talker. We also find that participants who have undergone more musical training show better performance on both verbal and non-verbal selective attention tasks, and this musician advantage is greater in older participants. This suggests that one source of a potential musician advantage for speech perception in complex environments may be experience or skill in directing and maintaining attention to a single auditory object

Tailored perception: individuals’ speech and music perception strategies fit their perceptual abilities

Perception involves integration of multiple dimensions that often serve overlapping, redundant functions, e.g. pitch, duration, and amplitude in speech. Individuals tend to prioritize these dimensions differently (stable, individualized perceptual ‘strategies’) but the reason for this has remained unclear. Here we show that perceptual strategies relate to perceptual abilities. In a speech cue weighting experiment (trial N = 990), we first demonstrate that individuals with a severe deficit for pitch perception (congenital amusics; N=11) categorize linguistic stimuli similarly to controls (N=11) when the main distinguishing cue is duration, which they perceive normally. In contrast, in a prosodic task where pitch cues are the main distinguishing factor, we show that amusics place less importance on pitch and instead rely more on duration cues—even when pitch differences in the stimuli were large enough for amusics to discern. In a second experiment testing musical and prosodic phrase interpretation (N=16 amusics; 15 controls), we found that relying on duration allowed amusics to overcome their pitch deficits to perceive speech and music successfully. We conclude that auditory signals, because of their redundant nature, are robust to impairments for specific dimensions, and that optimal speech and music perception strategies depend not only on invariant acoustic dimensions (the physical signal), but on perceptual dimensions whose precision varies across individuals. Computational models of speech perception (indeed, all types of perception involving redundant cues e.g. vision and touch) should therefore aim to account for the precision of perceptual dimensions and characterize individuals as well as groups

Neural representation of vowel formants in tonotopic auditory cortex

Speech sounds are encoded by distributed patterns of activity in bilateral superior temporal cortex. However, it is unclear whether speech sounds are topographically represented in cortex, or which acoustic or phonetic dimensions might be spatially mapped. Here, using functional MRI, we investigated the potential spatial representation of vowels, which are largely distinguished from one another by the frequencies of their first and second formants, i.e. peaks in their frequency spectra. This allowed us to generate clear hypotheses about the representation of specific vowels in tonotopic regions of auditory cortex. We scanned participants as they listened to multiple natural tokens of the vowels [ɑ] and [i], which we selected because their first and second formants overlap minimally. Formant-based regions of interest were defined for each vowel based on spectral analysis of the vowel stimuli and independently acquired tonotopic maps for each participant. We found that perception of [ɑ] and [i] yielded differential activation of tonotopic regions corresponding to formants of [ɑ] and [i], such that each vowel was associated with increased signal in tonotopic regions corresponding to its own formants. This pattern was observed in Heschl’s gyrus and the superior temporal gyrus, in both hemispheres, and for both the first and second formants. Using linear discriminant analysis of mean signal change in formant-based regions of interest, the identity of untrained vowels was predicted with ~73% accuracy. Our findings show that cortical encoding of vowels is scaffolded on tonotopy, a fundamental organizing principle of auditory cortex that is not language-specific

Non-invasive laminar inference with MEG: comparison of methods and source inversion algorithms

Magnetoencephalography (MEG) is a direct measure of neuronal current flow; its anatomical resolution is therefore not constrained by physiology but rather by data quality and the models used to explain these data. Recent simulation work has shown that it is possible to distinguish between signals arising in the deep and superficial cortical laminae given accurate knowledge of these surfaces with respect to the MEG sensors. This previous work has focused around a single inversion scheme (multiple sparse priors) and a single global parametric fit metric (free energy). In this paper we use several different source inversion algorithms and both local and global, as well as parametric and non-parametric fit metrics in order to demonstrate the robustness of the discrimination between layers. We find that only algorithms with some sparsity constraint can successfully be used to make laminar discrimination. Importantly, local t-statistics, global cross-validation and free energy all provide robust and mutually corroborating metrics of fit. We show that discrimination accuracy is affected by patch size estimates, cortical surface features, and lead field strength, which suggests several possible future improvements to this technique. This study demonstrates the possibility of determining the laminar origin of MEG sensor activity, and thus directly testing theories of human cognition that involve laminar- and frequency-specific mechanisms. This possibility can now be achieved using recent developments in high precision MEG, most notably the use of subject-specific head-casts, which allow for significant increases in data quality and therefore anatomically precise MEG recordings