Samantha W. Michalka

Auditory Spatial Attention Representations in the Human Cerebral Cortex

Auditory spatial attention serves important functions in auditory source separation and selection. Although auditory spatial attention mechanisms have been generally investigated, the neural substrates encoding spatial information acted on by attention have not been identified in the human neocortex. We performed functional magnetic resonance imaging experiments to identify cortical regions that support auditory spatial attention and to test 2 hypotheses regarding the coding of auditory spatial attention: 1) auditory spatial attention might recruit the visuospatial maps of the intraparietal sulcus (IPS) to create multimodal spatial attention maps; 2) auditory spatial information might be encoded without explicit cortical maps. We mapped visuotopic IPS regions in individual subjects and measured auditory spatial attention effects within these regions of interest. Contrary to the multimodal map hypothesis, we observed that auditory spatial attentional modulations spared the visuotopic maps of IPS; the parietal regions activated by auditory attention lacked map structure. However, multivoxel pattern analysis revealed that the superior temporal gyrus and the supramarginal gyrus contained significant information about the direction of spatial attention. These findings support the hypothesis that auditory spatial information is coded without a cortical map representation. Our findings suggest that audiospatial and visuospatial attention utilize distinctly different spatial coding schemes.

Short-Term Memory for Space and Time Flexibly Recruit Complementary Sensory-Biased Frontal Lobe Attention Networks

The frontal lobes control wide-ranging cognitive functions; however, functional subdivisions of human frontal cortex are only coarsely mapped. Here, functional magnetic resonance imaging reveals two distinct visual-biased attention regions in lateral frontal cortex, superior precentral sulcus (sPCS) and inferior precentral sulcus (iPCS), anatomically interdigitated with two auditory-biased attention regions, transverse gyrus intersecting precentral sulcus (tgPCS) and caudal inferior frontal sulcus (cIFS). Intrinsic functional connectivity analysis demonstrates that sPCS and iPCS fall within a broad visual-attention network, while tgPCS and cIFS fall within a broad auditory-attention network. Interestingly, we observe that spatial and temporal short-term memory (STM), respectively, recruit visual and auditory attention networks in the frontal lobe, independent of sensory modality. These findings not only demonstrate that both sensory modality and information domain influence frontal lobe functional organization, they also demonstrate that spatial processing co-localizes with visual processing and that temporal processing co-localizes with auditory processing in lateral frontal cortex.

Cognitive Control Network Contributions to Memory-Guided Visual Attention

Visual attentional capacity is severely limited, but humans excel in familiar visual contexts, in part because long-term memories guide efficient deployment of attention. To investigate the neural substrates that support memory-guided visual attention, we performed a set of functional MRI experiments that contrast long-term, memory-guided visuospatial attention with stimulus-guided visuospatial attention in a change detection task. Whereas the dorsal attention network was activated for both forms of attention, the cognitive control network(CCN) was preferentially activated during memory-guided attention. Three posterior nodes in the CCN, posterior precuneus, posterior callosal sulcus/mid-cingulate, and lateral intraparietal sulcus exhibited the greatest specificity for memory-guided attention. These 3 regions exhibit functional connectivity at rest, and we propose that they form a subnetwork within the broader CCN. Based on the task activation patterns, we conclude that the nodes of this subnetwork are preferentially recruited for long-term memory guidance of visuospatial attention.

Auditory Spatial Coding Flexibly Recruits Anterior, but Not Posterior, Visuotopic Parietal Cortex

Audition and vision both convey spatial information about the environment, but much less is known about mechanisms of auditory spatial cognition than visual spatial cognition. Human cortex contains >20 visuospatial map representations but no reported auditory spatial maps. The intraparietal sulcus (IPS) contains several of these visuospatial maps, which support visuospatial attention and short-term memory (STM). Neuroimaging studies also demonstrate that parietal cortex is activated during auditory spatial attention and working memory tasks, but prior work has not demonstrated that auditory activation occurs within visual spatial maps in parietal cortex. Here, we report both cognitive and anatomical distinctions in the auditory recruitment of visuotopically mapped regions within the superior parietal lobule. An auditory spatial STM task recruited anterior visuotopic maps (IPS2–4, SPL1), but an auditory temporal STM task with equivalent stimuli failed to drive these regions significantly. Behavioral and eye-tracking measures rule out task difficulty and eye movement explanations. Neither auditory task recruited posterior regions IPS0 or IPS1, which appear to be exclusively visual. These findings support the hypothesis of multisensory spatial processing in the anterior, but not posterior, superior parietal lobule and demonstrate that recruitment of these maps depends on auditory task demands.

Shared filtering processes link attentional and visual short-term memory capacity limits.

Both visual attention and visual short-term memory (VSTM) have been shown to have capacity limits of 4 ± 1 objects, driving the hypothesis that they share a visual processing buffer. However, these capacity limitations also show strong individual differences, making the degree to which these capacities are related unclear. Moreover, other research has suggested a distinction between attention and VSTM buffers. To explore the degree to which capacity limitations reflect the use of a shared visual processing buffer, we compared individual subjects capacities on attentional and VSTM tasks completed in the same testing session. We used a multiple object tracking (MOT) and a VSTM change detection task, with varying levels of distractors, to measure capacity. Significant correlations in capacity were not observed between the MOT and VSTM tasks when distractor filtering demands differed between the tasks. Instead, significant correlations were seen when the tasks shared spatial filtering demands. Moreover, these filtering demands impacted capacity similarly in both attention and VSTM tasks. These observations fail to support the view that visual attention and VSTM capacity limits result from a shared buffer but instead highlight the role of the resource demands of underlying processes in limiting capacity.

Influences of Long-Term Memory-Guided Attention and Stimulus-Guided Attention on Visuospatial Representations within Human Intraparietal Sulcus.

Human parietal cortex plays a central role in encoding visuospatial information and multiple visual maps exist within the intraparietal sulcus (IPS), with each hemisphere symmetrically representing contralateral visual space. Two forms of hemispheric asymmetries have been identified in parietal cortex ventrolateral to visuotopic IPS. Key attentional processes are localized to right lateral parietal cortex in the temporoparietal junction and long-term memory (LTM) retrieval processes are localized to the left lateral parietal cortex in the angular gyrus. Here, using fMRI, we investigate how spatial representations of visuotopic IPS are influenced by stimulus-guided visuospatial attention and by LTM-guided visuospatial attention. We replicate prior findings that a hemispheric asymmetry emerges under stimulus-guided attention: in the right hemisphere (RH), visual maps IPS0, IPS1, and IPS2 code attentional targets across the visual field; in the left hemisphere (LH), IPS0-2 codes primarily contralateral targets. We report the novel finding that, under LTM-guided attention, both RH and LH IPS0-2 exhibit bilateral responses and hemispheric symmetry re-emerges. Therefore, we demonstrate that both hemispheres of IPS0-2 are independently capable of dynamically changing spatial coding properties as attentional task demands change. These findings have important implications for understanding visuospatial and memory-retrieval deficits in patients with parietal lobe damage. SIGNIFICANCE STATEMENT The human parietal lobe contains multiple maps of the external world that spatially guide perception, action, and cognition. Maps in each cerebral hemisphere code information from the opposite side of space, not from the same side, and the two hemispheres are symmetric. Paradoxically, damage to specific parietal regions that lack spatial maps can cause patients to ignore half of space (hemispatial neglect syndrome), but only for right (not left) hemisphere damage. Conversely, the left parietal cortex has been linked to retrieval of vivid memories regardless of space. Here, we investigate possible underlying mechanisms in healthy individuals. We demonstrate two forms of dynamic changes in parietal spatial representations: an asymmetric one for stimulus-guided attention and a symmetric one for long-term memory-guided attention.

Structural and functional connectivity of visual and auditory attentional networks: insights from the Human Connectome Project

Recent work in our laboratory has suggested that human caudal lateral frontal cortex contains four interleaved regions in each hemisphere that exhibit strong sensory-specific biases in attention tasks (Michalka et al, 2014). Two visually-biased attention regions, superior and inferior pre-central sulcus (sPCS, iPCS), anatomically alternate with two auditory-biased attention regions, caudal inferior frontal sulcus (cIFS) and the transverse gyrus intersection the precentral sulcus (tgPCS). These small regions were identified in fMRI studies in a small number of individual subjects. Here, we have investigated these regions and their putative networks by mining the WashU-Minn Human Connectome Project (HCP) dataset. We used data from the 482 HCP participants with both diffusion-weighted imaging and resting-state fMRI. We defined seed regions from our individual subject data in a task that contrasted auditory and visual spatial attention. Probabilistic activation maps were constructed and thresholded to generate ROIs. These ROIs served as seed regions for resting state and tractography analyses of the HCP dataset. Stronger functional connectivity was observed for the sPCS and iPCS than for tgPCS and cIFS with superior parietal lobule visual attention regions, and conversely stronger connectivity was observed for the tgPCS and cIFS than for sPCS and iPCS with superior temporal lobe auditory attention regions. A similar pattern was observed with tractography for all ROIs, except for tgPCS. We next analyzed the whole-brain connectivity patterns of these ROIs using a multivariate approach; we found that the modality of sensory-bias can be predicted well above chance in both hemispheres at a voxelwise scale (L:71%, R:80%), using only the connectivity pattern of an individual voxel. A long-term goal of this analysis is to develop reliable methods for identifying fine-scale brain networks in large population datasets, which could have important clinical applications. Our preliminary results reveal both successes and challenges of these efforts. Meeting abstract presented at VSS 2015.

Sensory-biased and multiple-demand processing in human lateral frontal cortex.

The functionality of much of human lateral frontal cortex (LFC) has been characterized as “multiple demand” (MD) as these regions appear to support a broad range of cognitive tasks. In contrast to this domain-general account, recent evidence indicates that portions of LFC are consistently selective for sensory modality. Michalka et al. (2015) reported two bilateral regions that are biased for visual attention, superior precentral sulcus (sPCS) and inferior precentral sulcus (iPCS), interleaved with two bilateral regions that are biased for auditory attention, transverse gyrus intersecting precentral sulcus (tgPCS) and caudal inferior frontal sulcus (cIFS). In the present study, we use fMRI to examine both the multiple-demand and sensory-bias hypotheses within caudal portions of human LFC (both men and women participated). Using visual and auditory 2-back tasks, we replicate the finding of two bilateral visual-biased and two bilateral auditory-biased LFC regions, corresponding to sPCS and iPCS and to tgPCS and cIFS, and demonstrate high within-subject reliability of these regions over time and across tasks. In addition, we assess MD responsiveness using BOLD signal recruitment and multi-task activation indices. In both, we find that the two visual-biased regions, sPCS and iPCS, exhibit stronger MD responsiveness than do the auditory-biased LFC regions, tgPCS and cIFS; however, neither reaches the degree of MD responsiveness exhibited by dorsal anterior cingulate/presupplemental motor area or by anterior insula. These results reconcile two competing views of LFC by demonstrating the coexistence of sensory specialization and MD functionality, especially in visual-biased LFC structures. SIGNIFICANCE STATEMENT Lateral frontal cortex (LFC) is known to play a number of critical roles in supporting human cognition; however, the functional organization of LFC remains controversial. The “multiple demand” (MD) hypothesis suggests that LFC regions provide domain-general support for cognition. Recent evidence challenges the MD view by demonstrating that a preference for sensory modality, vision or audition, defines four discrete LFC regions. Here, the sensory-biased LFC results are reproduced using a new task, and MD responsiveness of these regions is tested. The two visual-biased regions exhibit MD behavior, whereas the auditory-biased regions have no more than weak MD responses. These findings help to reconcile two competing views of LFC functional organization.

Sensory-biased attention networks in human lateral frontal cortex revealed by intrinsic functional connectivity

&NA; Human frontal cortex is commonly described as being insensitive to sensory modality, however several recent studies cast doubt on this view. Our laboratory previously reported two visual‐biased attention regions interleaved with two auditory‐biased attention regions, bilaterally, within lateral frontal cortex. These regions selectively formed functional networks with posterior visual‐biased and auditory‐biased attention regions. Here, we conducted a series of functional connectivity analyses to validate and expand this analysis to 469 subjects from the Human Connectome Project (HCP). Functional connectivity analyses replicated the original findings and revealed a novel hemispheric connectivity bias. We also subdivided lateral frontal cortex into 21 thin‐slice ROIs and observed bilateral patterns of spatially alternating visual‐biased and auditory‐biased attention network connectivity. Finally, we performed a correlation difference analysis that revealed five additional bilateral lateral frontal regions differentially connected to either the visual‐biased or auditory‐biased attention networks. These findings leverage the HCP dataset to demonstrate that sensory‐biased attention networks may have widespread influence in lateral frontal cortical organization. Graphical abstract Figure. No caption available. HighlightsSensory‐biased attention networks extend into human lateral frontal cortex (LFC).Small N dataset used to mine Human Connectome Project dataset (N = 469).RS‐functional connectivity confirms 4 sensory‐biased LFC regions bilaterally.5 new putative sensory‐biased attention regions observed bilaterally in LFC.

Prediction of individualized task activation in sensory modality-selective frontal cortex with ‘connectome fingerprinting’

&NA; The human cerebral cortex is estimated to comprise 200–300 distinct functional regions per hemisphere. Identification of the precise anatomical location of an individuals unique set of functional regions is a challenge for neuroscience that has broad scientific and clinical utility. Recent studies have demonstrated the existence of four interleaved regions in lateral frontal cortex (LFC) that are part of broader visual attention and auditory attention networks (Michalka et al., 2015; Noyce et al., 2017; Tobyne et al., 2017). Due to a large degree of inter‐subject anatomical variability, identification of these regions depends critically on within‐subject analyses. Here, we demonstrate that, for both sexes, an individuals unique pattern of resting‐state functional connectivity can accurately identify their specific pattern of visual‐ and auditory‐selective working memory and attention task activation in lateral frontal cortex (LFC) using “connectome fingerprinting.” Building on prior techniques (Saygin et al., 2011; Osher et al., 2016; Tavor et al., 2016; Smittenaar et al., 2017; Wang et al., 2017; Parker Jones et al., 2017), we demonstrate here that connectome fingerprint predictions are far more accurate than group‐average predictions and match the accuracy of within‐subject task‐based functional localization, while requiring less data. These findings are robust across brain parcellations and are improved with penalized regression methods. Because resting‐state data can be easily and rapidly collected, these results have broad implications for both clinical and research investigations of frontal lobe function. Our findings also provide a set of recommendations for future research.