Maya L. Rosen

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.

Long-term memory guidance of visuospatial attention in a change-detection paradigm

Visual task performance is generally stronger in familiar environments. One reason for this familiarity benefit is that we learn where to direct our visual attention and effective attentional deployment enhances performance. Visual working memory plays a central role in supporting long-term memory guidance of visuospatial attention. We modified a change detection task to create a new paradigm for investigating long-term memory guidance of attention. During the training phase, subjects viewed images in a flicker paradigm and were asked to detect between one and three changes in the images. The test phase required subjects to detect a single change in a one-shot change detection task in which they held all possible locations of changes in visual working memory and deployed attention to those locations to determine if a change occurred. Subjects detected significantly more changes in images for which they had been trained to detect the changes, demonstrating that memory of the images guided subjects in deploying their attention. Moreover, capacity to detect changes was greater for images that had multiple changes during the training phase. In Experiment 2, we observed that capacity to detect changes for the 3-studied change condition increased significantly with more study exposures and capacity was significantly higher than 1, indicating that subjects were able to attend to more than one location. Together, these findings suggest memory and attentional systems interact via working memory such that long-term memory can be used to direct visual spatial attention to multiple locations based on previous experience.

Functional correlates of optic flow motion processing in Parkinson's disease.

The visual input created by the relative motion between an individual and the environment, also called optic flow, influences the sense of self-motion, postural orientation, veering of gait, and visuospatial cognition. An optic flow network comprising visual motion areas V6, V3A, and MT+, as well as visuo-vestibular areas including posterior insula vestibular cortex (PIVC) and cingulate sulcus visual area (CSv), has been described as uniquely selective for parsing egomotion depth cues in humans. Individuals with Parkinson’s disease (PD) have known behavioral deficits in optic flow perception and visuospatial cognition compared to age- and education-matched control adults (MC). The present study used functional magnetic resonance imaging (fMRI) to investigate neural correlates related to impaired optic flow perception in PD. We conducted fMRI on 40 non-demented participants (23 PD and 17 MC) during passive viewing of simulated optic flow motion and random motion. We hypothesized that compared to the MC group, PD participants would show abnormal neural activity in regions comprising this optic flow network. MC participants showed robust activation across all regions in the optic flow network, consistent with studies in young adults, suggesting intact optic flow perception at the neural level in healthy aging. PD participants showed diminished activity compared to MC particularly within visual motion area MT+ and the visuo-vestibular region CSv. Further, activation in visuo-vestibular region CSv was associated with disease severity. These findings suggest that behavioral reports of impaired optic flow perception and visuospatial performance may be a result of impaired neural processing within visual motion and visuo-vestibular regions in PD.

Hippocampal contribution to context encoding across development is disrupted following early-life adversity

Context can drastically influence responses to environmental stimuli. For example, a gunshot should provoke a different response at a public park than a shooting range. Little is known about how contextual processing and neural correlates change across human development or about individual differences related to early environmental experiences. Children (N = 60; 8–19 years, 24 exposed to interpersonal violence) completed a context encoding task during fMRI scanning using a delayed match-to-sample design with neutral, happy, and angry facial cues embedded in realistic background scenes. Outside the scanner, participants completed a memory test for context-face pairings. Context memory and neural correlates of context encoding did not vary with age. Larger hippocampal volume was associated with better context memory. Posterior hippocampus was recruited during context encoding, and greater activation in this region predicted better memory for contexts paired with angry faces. Children exposed to violence had poor memory of contexts paired with angry faces, reduced hippocampal volume, and atypical neural recruitment on encoding trials with angry faces, including reduced hippocampal activation and greater functional connectivity between hippocampus and ventrolateral prefrontal cortex (vlPFC). Greater hippocampus-vlPFC connectivity was associated with worse memory for contexts paired with angry faces. Posterior hippocampus appears to support context encoding, a process that does not exhibit age-related variation from middle childhood to late adolescence. Exposure to dangerous environments in childhood is associated with poor context encoding in the presence of threat, likely due to greater vlPFC-dependent attentional narrowing on threat cues at the expense of hippocampus-dependent processing of the broader context. SIGNIFICANCE STATEMENT The ability to use context to guide reactions to environmental stimuli promotes flexible behavior. Remarkably little research has examined how contextual processing changes across development or about influences of the early environment. We provide evidence for posterior hippocampus involvement in context encoding in youth and lack of age-related variation from middle childhood to late adolescence. Children exposed to interpersonal violence exhibited poor memory of contexts paired with angry faces and atypical neural recruitment during context encoding in the presence of threatening facial cues. Heightened attention to threat following violence exposure may come at the expense of encoding contextual information, which may ultimately contribute to pathological fear expressed in safe contexts.

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.

Socioeconomic disparities in academic achievement: A multi-modal investigation of neural mechanisms in children and adolescents

&NA; Growing evidence suggests that childhood socioeconomic status (SES) influences neural development, which may contribute to the well‐documented SES‐related disparities in academic achievement. However, the particular aspects of SES that impact neural structure and function are not well understood. Here, we investigate associations of childhood SES and a potential mechanism—degree of cognitive stimulation in the home environment—with cortical structure, white matter microstructure, and neural function during a working memory (WM) task across development. Analyses included 53 youths (age 6–19 years). Higher SES as reflected in the income‐to‐needs ratio was associated with higher parent‐reported achievement, WM performance, and cognitive stimulation in the home environment. Although SES was not significantly associated with cortical thickness, children raised in more cognitively stimulating environments had thicker cortex in the frontoparietal network and cognitive stimulation mediated the assocation between SES and cortical thickness in the frontoparietal network. Higher family SES was associated with white matter microstructure and neural activation in the frontoparietal network during a WM task, including greater fractional anisotropy (FA) in the right and left superior longitudinal fasciculi (SLF), and greater BOLD activation in multiple regions of the prefrontal cortex during WM encoding and maintenance. Greater FA and activation in these regions was associated higher parent‐reported achievement. Together, cognitive stimulation, WM performance, FA in the SLF, and prefrontal activation during WM encoding and maintenance significantly mediated the association between SES and parent‐reported achievement. These findings highlight potential neural, cognitive, and environmental mechanisms linking SES with academic achievement and suggest that enhancing cognitive stimulation in the home environment might be one effective strategy for reducing SES‐related disparities in academic outcomes. HighlightsHighlight multiple links between SES and frontoparietal network structure and function.Provide evidence for link between cognitive enrichment and frontoparietal structure.Highlight neural, cognitive and environmental mechanism linking SES and academic achievement.

Cerebellar Contributions to Visual Attention and Visual Working Memory Revealed by Functional MRI and Intrinsic Functional Connectivity.

The study of cerebellum function has been traditionally limited to the motor domain. Recent research, however, has begun to characterize the cerebellums role in cognition (see Schmahmann, 2010) and has demonstrated intrinsic functional connectivity between cerebral cortical networks and distinct cerebellar regions (Buckner et al., 2011). Here, in two separate fMRI experiments, we investigated whether cerebro-cerebellar connectivity of dorsal attention network (DAN) predicts cerebellar activation during visual attention and visual working memory (VWM) task performance. In experiment 1 (N=8), subjects performed a multiple-object tracking task. In experiment 2 (N=9), subjects performed a VWM change detection task using oriented bars. Memory load was varied across blocks (set size: SS0, SS1, or SS4). Both experiments employed resting-state functional connectivity analysis using cortical network seeds (Yeo et al., 2011) to parcellate cerebro-cerebellar networks in individual subjects. In experiment 1, a region-of-interest analysis revealed a robust attentional effect within cerebellar regions functionally connected to the cortical DAN (p< .01). Conversely, cerebellar regions functionally connected to the cortical default mode network (DMN) showed reliable deactivation (p< .001). In experiment 2, contrasting SS4 with SS0 and SS1 resulted in a similar pattern of competitive interaction between cerebellar nodes of the DAN and DMN. Load-dependent activation spatially corresponded with cerebellar DAN nodes (SS4-SS0: p< .005; SS4-SS1: p< .0001) and load-dependent deactivation was observed within cerebellar DMN nodes (SS4-SS0: p< .005; SS4-SS1: p< .0005). Across both experiments the strength of intrinsic functional connectivity, with either the cortical DAN or the cortical DMN, significantly predicted the response of individual cerebellar voxels (Experiment 1: rDAN =.67, rDMN =-.71; Experiment 2: rDAN =.60, rDMN =-.56). Our results indicate that cerebellar nodes of the DAN contribute to network function across a diverse range of attentive and working memory conditions. Meeting abstract presented at VSS 2015.