Kathryn J. Devaney

Scene-Selective Cortical Regions in Human and Nonhuman Primates

fMRI studies have revealed three scene-selective regions in human visual cortex [the parahippocampal place area (PPA), transverse occipital sulcus (TOS), and retrosplenial cortex (RSC)], which have been linked to higher-order functions such as navigation, scene perception/recognition, and contextual association. Here, we document corresponding (presumptively homologous) scene-selective regions in the awake macaque monkey, based on direct comparison to human maps, using identical stimuli and largely overlapping fMRI procedures. In humans, our results showed that the three scene-selective regions are centered near—but distinct from—the gyri/sulci for which they were originally named. In addition, all these regions are located within or adjacent to known retinotopic areas. Human RSC and PPA are located adjacent to the peripheral representation of primary and secondary visual cortex, respectively. Human TOS is located immediately anterior/ventral to retinotopic area V3A, within retinotopic regions LO-1, V3B, and/or V7. Mirroring the arrangement of human regions fusiform face area (FFA) and PPA (which are adjacent to each other in cortex), the presumptive monkey homolog of human PPA is located adjacent to the monkey homolog of human FFA, near the posterior superior temporal sulcus. Monkey TOS includes the region predicted from the human maps (macaque V4d), extending into retinotopically defined V3A. A possible monkey homolog of human RSC lies in the medial bank, near peripheral V1. Overall, our findings suggest a homologous neural architecture for scene-selective regions in visual cortex of humans and nonhuman primates, analogous to the face-selective regions demonstrated earlier in these two species.

Lower-Level Stimulus Features Strongly Influence Responses in the Fusiform Face Area

An intriguing region of human visual cortex (the fusiform face area; FFA) responds selectively to faces as a general higher-order stimulus category. However, the potential role of lower-order stimulus properties in FFA remains incompletely understood. To clarify those lower-level influences, we measured FFA responses to independent variation in 4 lower-level stimulus dimensions using standardized face stimuli and functional Magnetic Resonance Imaging (fMRI). These dimensions were size, position, contrast, and rotation in depth (viewpoint). We found that FFA responses were strongly influenced by variations in each of these image dimensions; that is, FFA responses were not “invariant” to any of them. Moreover, all FFA response functions were highly correlated with V1 responses (r = 0.95–0.99). As in V1, FFA responses could be accurately modeled as a combination of responses to 1) local contrast plus 2) the cortical magnification factor. In some measurements (e.g., face size or a combinations of multiple cues), the lower-level variations dominated the range of FFA responses. Manipulation of lower-level stimulus parameters could even change the category preference of FFA from “face selective” to “object selective.” Altogether, these results emphasize that a significant portion of the FFA response reflects lower-level visual responses.

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.

fMRI mapping of a morphed continuum of 3D shapes within inferior temporal cortex.

Here, we mapped fMRI responses to incrementally changing shapes along a continuous 3D morph, ranging from a head (“face”) to a house (“place”). The response to each shape was mapped independently by using single-stimulus imaging, and stimulus shapes were equated for lower-level visual cues. We measured activity in 2-mm samples across human inferior temporal cortex from the fusiform face area (FFA) (apparently selective for faces) to the parahippocampal place area (PPA) (apparently selective for places), testing for (i) incremental changes in the topography of FFA and PPA (predicted by the continuous-mapping model) or (ii) little or no response to the intermediate morphed shapes (predicted by the category model). Neither result occurred; instead, we found approximately linearly graded changes in the response amplitudes to graded-shape changes, without changes in topography—similar to visual responses in different lower-tier cortical areas.

Spatial encoding and underlying circuitry in scene-selective cortex

Three cortical areas (Retro-Splenial Cortex (RSC), Transverse Occipital Sulcus (TOS) and Parahippocampal Place Area (PPA)) respond selectively to scenes. However, their wider role in spatial encoding and their functional connectivity remain unclear. Using fMRI, first we tested the responses of these areas during spatial comparison tasks using dot targets on white noise. Activity increased during task performance in both RSC and TOS, but not in PPA. However, the amplitude of task-driven activity and behavioral measures of task demand were correlated only in RSC. A control experiment showed that none of these areas were activated during a comparable shape comparison task. Secondly, we analyzed functional connectivity of these areas during the resting state. Results revealed a significant connection between RSC and frontal association areas (known to be involved in perceptual decision-making). In contrast, TOS showed functional connections dorsally with the Inferior Parietal Sulcus, and ventrally with the Lateral Occipital Complex--but not with RSC and/or frontal association areas. Moreover, RSC and TOS showed differentiable functional connections with the anterior-medial and posterior-lateral parts of PPA, respectively. These results suggest two parallel pathways for spatial encoding, including RSC and TOS respectively. Only the RSC network was involved in active spatial comparisons.

FMRI analysis of contrast polarity in face-selective cortex in humans and monkeys

Recognition is strongly impaired when the normal contrast polarity of faces is reversed. For instance, otherwise-familiar faces become very difficult to recognize when viewed as photographic negatives. Here, we used fMRI to demonstrate related properties in visual cortex: 1) fMRI responses in the human Fusiform Face Area (FFA) decreased strongly (26%) to contrast-reversed faces across a wide range of contrast levels (5.3-100% RMS contrast), in all subjects tested. In a whole brain analysis, this contrast polarity bias was largely confined to the Fusiform Face Area (FFA; p<0.0001), with possible involvement of a left occipital face-selective region. 2) It is known that reversing facial contrast affects three image properties in parallel (absorbance, shading, and specular reflection). Here, comparison of FFA responses to those in V1 suggests that the contrast polarity bias is produced in FFA only when all three component properties were reversed simultaneously, which suggests a prominent non-linearity in FFA processing. 3) Across a wide range (180°) of illumination source angles, 3D face shapes without texture produced response constancy in FFA, without a contrast polarity bias. 4) Consistent with psychophysics, analogous fMRI biases for normal contrast polarity were not produced by non-face objects, with image statistics similar to the face stimuli. 5) Using fMRI, we also demonstrated a contrast polarity bias in awake behaving macaque monkeys, in the cortical region considered homologous to human FFA. Thus common cortical mechanisms may underlie facial contrast processing across ~25 million years of primate evolution.

Characterizing Visual Field Deficits in Cerebral/Cortical Visual Impairment (CVI) Using Combined Diffusion Based Imaging and Functional Retinotopic Mapping: A Case Study

Cortical/cerebral visual impairment (CVI) is the leading cause of pediatric visual impairment in children in developed countries and has become a significant public health concern (Kong et al., 2012). CVI is clinically defined as significant visual dysfunction resulting primarily from perinatal injury to visual pathways and structures rather than ocular pathology alone (Dutton, 2003). Perinatal hypoxia is the most common cause resulting in impaired maturation of key visual pathways such as the optic radiations; a general condition referred to as white matter damage of immaturity (WMDI). In preterm infants, this maldevelopment is often associated with periventricular leukomalacia (PVL), which is characterized by an enlargement of the lateral ventricles and focal gliosis of surrounding white matter pathways coursing on to the visual cortex (Good et al., 2001; Hoyt, 2007). Depending on the location and extent of the damage, children with CVI often present with a broad range and combination of visual dysfunctions such as decreased visual acuity, visual field deficits, and also impairments in oculomotor, visuomotor, and cognitive visual processing (Good et al., 2001; Dutton, 2003; Hoyt, 2007). The variability in the location and extent of brain injury across individuals makes the prediction of visual functional outcomes and recovery in CVI patients particularly challenging (McKillop and Dutton, 2008). Despite the increasing prevalence of this condition, the relationship between observed visual deficits in CVI and the underlying structural and functional changes resulting from damage to key visual pathways, remains poorly understood. Specifically, it remains unknown how the maldevelopment of key visual pathways relates to the organization of the visual cortex and further, how these structural and functional changes relate to visual impairments observed within the clinical setting. Standard clinical neuroimaging techniques such as computerized tomography (CT) and magnetic resonance imaging (MRI) can help characterize gross changes in cerebral structure. However, the underlying micro-architecture of key white matter pathways (such as the optic radiations) cannot be fully ascertained, nor can the function of visual cortical areas be assessed. Advances in diffusion based imaging (i.e., diffusion MRI) modalities such as high angular resolution diffusion based imaging (HARDI) combined with tractography analysis techniques can be used to reveal the organization of specific white matter projections (Jones, 2008) see also (Ffytche et al., 2010). At the same time, retinotopic mapping using functional magnetic resonance imaging (fMRI) can be employed to assess the organizational and functional integrity of early visual cortical areas (Wandell, 1999). In this study, we used a combined structural and functional multi-modal neuroimaging approach to characterize the underlying maldevelopment of the geniculo-striate pathway in an adolescent with CVI. The patient presented here had a documented inferior visual field deficit determined on clinical ophthalmic examination. Despite her diagnosis of CVI and associated visual impairments, she was able to participate in formal testing and provide reliable data (including maintaining fixation during perimetry and retinotopic stimulation) and also remain immobile in the scanner environment without the need of anesthesia. Thus, (and contrary to prior imaging studies with CVI individuals), we had the opportunity to obtain high quality structural and functional imaging data on the same subject in order to investigate the relationship between the structural integrity of the optic radiations and the functional organization of early visual cortical areas with respect to her clinical visual field impairment. We demonstrate the feasibility of combining this structural and functional imaging approach in a patient with CVI along with an age/gender matched normal developed control for comparison. By combining these imaging modalities, it is possible to provide further insight regarding the functional manifestations of early onset developmental damage to key visual pathways and their relation to specific impairments of visual function.

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.

Functional MRI Reveals a Cognitive Control Subnetwork Supporting Long-Term Memory-Guided Visual Attention

Human visual performance exceeds that of powerful supercomputers. Paradoxically, human attentional capacity is extremely limited. We can reconcile this superior performance with our limited attentional capacity by taking into account the important role of long-term memory, which guides attention to the most relevant information in an environment. Previous work from our laboratory (Rosen et al., in revision) has found that three regions located within the posterior Cognitive Control Network (defined-- using Yeo et al., 2011), including the lateral intraparietal sulcus (latIPS), posterior callosal sulcus (CaS-p), and the posterior precuneus (PrC-p) were more strongly recruited during long-term memory-guided attention compared to stimulus-guided attention. Recent work has suggested that these three regions form a subnetwork and a meta-analysis suggested that they support long-term memory retrieval (Power et al, 2011; 2014). It is unclear if this network plays a specific role in memory-guided attention or a more general role in memory retrieval. Here, we designed an experiment to directly contrast long-term memory-guided attention, stimulus-guided attention and long-term memory retrieval in the same subjects (n = 24). Subjects performed a cued target detection task with matched visual stimuli in all conditions. Cues either explicitly directed spatial attention, required subjects to use LTM to direct spatial attention or forced memory retrieval without spatial attention. All three regions of the subnetwork (PrC-p, CaS-p and latIPS) in both hemispheres showed the greatest activity in long-term memory-guided attention (allp > 0.01, corrected) with no regions showing differences between long-term memory retrieval and stimulus-guided conditions. Effects were strongly bilateral in PrC-p and CaS-p, but latIPS was more selective for memory-guided attention in the right hemisphere (Hemisphere:Condition interaction F(2,46) = 13.43, p< 0.001). We suggest that this subnetwork of posterior Cognitive Control Network nodes (PrC-p, CaS-p and latIPS) supports processing that integrates memory- and stimulus-based representations and is preferentially recruited for LTM-guided attention. Meeting abstract presented at VSS 2015.

Cortical and Subcortical Contributions to Long-Term Memory-Guided Visuospatial Attention

Long-term memory (LTM) helps to efficiently direct and deploy the scarce resources of the attentional system; however, the neural substrates that support LTM-guidance of visual attention are not well understood. Here, we present results from fMRI experiments that demonstrate that cortical and subcortical regions of a network defined by resting-state functional connectivity are selectively recruited for LTM-guided attention, relative to a similarly demanding stimulus-guided attention paradigm that lacks memory retrieval and relative to a memory retrieval paradigm that lacks covert deployment of attention. Memory-guided visuospatial attention recruited posterior callosal sulcus, posterior precuneus, and lateral intraparietal sulcus bilaterally. Additionally, 3 subcortical regions defined by intrinsic functional connectivity were recruited: the caudate head, mediodorsal thalamus, and cerebellar lobule VI/Crus I. Although the broad resting-state network to which these nodes belong has been referred to as a cognitive control network, the posterior cortical regions activated in the present study are not typically identified with supporting standard cognitive control tasks. We propose that these regions form a Memory-Attention Network that is recruited for processes that integrate mnemonic and stimulus-based representations to guide attention. These findings may have important implications for understanding the mechanisms by which memory retrieval influences attentional deployment.