Anthony Cate

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.

Perirhinal Cortex Contributes to Accuracy in Recognition Memory and Perceptual Discriminations

The prevailing view of the medial temporal lobe (MTL) holds that its structures are dedicated to long-term declarative memory. Recent evidence challenges this position, suggesting that perirhinal cortex (PRc) in the MTL may also play a role in perceptual discriminations of stimuli with substantial visual feature overlap. Relevant neuropsychological findings in humans have been inconclusive, likely because studies have relied on patients with large and variable MTL lesions. Here, we conducted a functional magnetic resonance imaging study in healthy individuals to determine whether PRc shows a performance-related involvement in perceptual oddball judgments that is comparable to its established role in recognition memory. Morphed faces were selected as stimuli because of their large degree of feature overlap. All trials involved presentation of displays with three faces. The perceptual oddball task required identification of the face least similar to the other display members. The memory task involved forced-choice recognition of a previously studied face. When levels of behavioral performance were matched, we observed comparable levels of activation in right PRc for both tasks. Moreover, right PRc activity differentiated between accurate and inaccurate trials in both tasks. Together these results indicate that declarative memory demands are not a prerequisite for a performance-related engagement of PRc and that the introduction of such declarative memory demands in an otherwise closely matched perceptual task does not necessarily lead to an increase in PRc involvement. As such our findings show that declarative memory and perception are not as clearly separable at the level of MTL functioning as traditionally thought.

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.

The role of apparent size in building- and object-specific regions of ventral visual cortex

Images of buildings and manipulable objects have been found to activate distinct regions in the ventral visual pathway. Yet, many non-categorical properties distinguish buildings from common everyday objects, and perhaps the most salient of these is size. In this fMRI study, we investigated whether or not changes in perceived scale can account for some of the differences in category-specific responses, independent of the influence of semantic or retinotopic image properties. We used independent scans to localize object-specific ROIs in lateral occipital cortex (LO) and scene-specific ROIs in the parahippocampal place area (PPA) and posterior collateral sulcus. We then contrasted the effects of stimulus category and perceived size/distance in these regions in a factorial design. Participants performed an oddball detection task while viewing images of objects, buildings, and planar rectangles both with and without a background that indicated stimulus size/distance via simple pictorial cues. The analyses of fMRI responses showed effects of perceived size/distance in addition to effects of category in LO and the PPA. Interestingly, when simple rectangles were presented in a control condition against the background that indicated size/distance, LO in the right hemisphere responded significantly more to the small/close rectangles than to the large/far ones, in spite of the fact that the rectangles themselves were identical. These findings suggest that ventral stream regions that show category specificity are modulated by the perceived size and distance of visual stimuli.

Spatial and temporal influences on extinction

This study investigated the spatial and temporal characteristics of the attentional deficit in patients exhibiting extinction to determine the extent to which these characteristics can be explained by a theory of an underlying gradient resulting from the differential contribution of interacting cell populations. The paradigm required the identification of two letters whose spatial location was varied both within and across hemifields. Additionally, the interval between the appearances of the two stimuli was manipulated by changing the stimulus onset asynchrony (SOA). A final variable, that of expectancy, was introduced by making the stimulus location more or less predictable and examining the effect of this top-down contingency on performance. The findings were consistent across two patients and indicated the joint contribution of both spatial and temporal factors: the contralesional stimulus was maximally extinguished when it was preceded by the ipsilesional stimulus by 300-900 ms, but this extinction was reduced when the stimuli appeared further ipsilesionally. Interestingly, there was increased extinction of the contralesional stimulus when location was predictable. These findings support the hypothesis that the attentional deficit in extinction patients arises from a contralesional-to-ipsilesional gradient of cell populations that interact in a mutually inhibitory manner.

Phonological Processing in Human Auditory Cortical Fields

We used population-based cortical-surface analysis of functional magnetic imaging data to characterize the processing of consonant–vowel–consonant syllables (CVCs) and spectrally matched amplitude-modulated noise bursts (AMNBs) in human auditory cortex as subjects attended to auditory or visual stimuli in an intermodal selective attention paradigm. Average auditory cortical field (ACF) locations were defined using tonotopic mapping in a previous study. Activations in auditory cortex were defined by two stimulus-preference gradients: (1) Medial belt ACFs preferred AMNBs and lateral belt and parabelt fields preferred CVCs. This preference extended into core ACFs with medial regions of primary auditory cortex (A1) and the rostral field preferring AMNBs and lateral regions preferring CVCs. (2) Anterior ACFs showed smaller activations but more clearly defined stimulus preferences than did posterior ACFs. Stimulus preference gradients were unaffected by auditory attention suggesting that ACF preferences reflect the automatic processing of different spectrotemporal sound features.

Distinct Patterns of Functional and Effective Connectivity between Perirhinal Cortex and Other Cortical Regions in Recognition Memory and Perceptual Discrimination

Traditionally, the medial temporal lobe (MTL) is thought to be dedicated to declarative memory. Recent evidence challenges this view, suggesting that perirhinal cortex (PrC), which interfaces the MTL with the ventral visual pathway, supports highly integrated object representations in recognition memory and perceptual discrimination. Even with comparable representational demands, perceptual and memory tasks differ in numerous task demands and the subjective experience they evoke. Here, we tested whether such differences are reflected in distinct patterns of connectivity between PrC and other cortical regions, including differential involvement of prefrontal control processes. We examined functional magnetic resonance imaging data for closely matched perceptual and recognition memory tasks for faces that engaged right PrC equivalently. Multivariate seed analyses revealed distinct patterns of interactions: Right ventrolateral prefrontal and posterior cingulate cortices exhibited stronger functional connectivity with PrC in recognition memory; fusiform regions were part of the pattern that displayed stronger functional connectivity with PrC in perceptual discrimination. Structural equation modeling revealed distinct patterns of effective connectivity that allowed us to constrain interpretation of these findings. Overall, they demonstrate that, even when MTL structures show similar involvement in recognition memory and perceptual discrimination, differential neural mechanisms are reflected in the interplay between the MTL and other cortical regions.

Hemispherically-Unified Surface Maps of Human Cerebral Cortex: Reliability and Hemispheric Asymmetries

Understanding the anatomical and structural organization of the cerebral cortex is facilitated by surface-based analysis enabled by FreeSurfer, Caret, and related tools. Here, we examine the precision of FreeSurfer parcellation of the cortex and introduce a method to align FreeSurfer-registered left and right hemispheres onto a common template in order to characterize hemispheric asymmetries. The results are visualized using Mollweide projections, an area-preserving map. The regional distribution, inter-hemispheric asymmetries and intersubject variability in cortical curvature, sulcal depth, cortical thickness, and cortical surface area of 138 young, right handed subjects were analyzed on the Mollweide projection map of the common spherical space. The results show that gyral and sulcal structures are aligned with high but variable accuracy in different cortical regions and show consistent hemispheric asymmetries that are maximal in posterior temporal regions.

Perceiving parts and shapes from concave surfaces

Abstract“A hole is nothing at all, but it can break your neck.” In a similar fashion to the danger illustrated by this folk paradox, concave regions pose difficulties to theories of visual shape perception. We can readily identify their shapes, but according to principles of how observers determine part boundaries, concavities in a planar surface should have very different figural shapes from the ones that we perceive. In three experiments, we tested the hypothesis that observers perceive local image features differently in simulated 3-D concave and convex regions but use them to arrive at similar shape percepts. Stimuli were shape-from-shading images containing regions that appeared either concave or convex in depth, depending on their orientation in the picture plane. The results show that concavities did not benefit from the same global object-based attention or holistic shape encoding as convexities and that the participants relied on separable spatial dimensions to judge figural shape in concavities. Concavities may exploit a secondary process for shape perception that allows regions composed of perceptually independent features to ultimately be perceived as gestalts.