Keith A. Schneider

Retinotopic Organization and Functional Subdivisions of the Human Lateral Geniculate Nucleus: A High-Resolution Functional Magnetic Resonance Imaging Study

Functional magnetic resonance imaging (fMRI) has provided intriguing insights into the topography and functional organization of visual cortical areas in the human brain. However, little is known about the functional anatomy of subcortical nuclei. Here, we used high-resolution fMRI (1.5 × 1.5 × 2 mm3) at 3 tesla to investigate the retinotopic organization of the human lateral geniculate nucleus (LGN). The central 15° of the visual field were mapped using periodic flickering checkerboard stimuli that evoked a traveling wave of activity. The contralateral visual hemifield was represented with the lower field in the medial-superior portion and the upper field in the lateral-inferior portion of each LGN. The horizontal meridian was significantly overrepresented relative to the vertical meridian. The fovea was represented in posterior and superior portions, with increasing eccentricities represented more anteriorly. The magnification of the fovea relative to the periphery was similar to that described for human primary visual cortex. The magnocellular regions of the LGN were distinguished based on their sensitivity to low stimulus contrast and tended to be located in its inferior and medial portions. Our results demonstrate striking similarities in the topographic organization of the macaque and human LGN and support accounts of a constant magnification from the retina through the cortex in both species.

Effects of Sustained Spatial Attention in the Human Lateral Geniculate Nucleus and Superior Colliculus

The role of subcortical visual structures such as the lateral geniculate nucleus (LGN) and the superior colliculus (SC) in the control of visual spatial attention remains poorly understood. Here, we used high-resolution functional magnetic resonance imaging to measure responses in the human LGN and SC during sustained spatial attention. Subjects covertly and continuously tracked one of two segments that rotated through the visual field, composed of either moving dots or transient colored shapes. Activity in both nuclei was generally enhanced by attention, independent of the stimulus type, with the voxels responding more sensitively to stimulus contrast (those dominated by magnocellular input) exhibiting greater attentional enhancement. The LGN contained clusters of voxels exhibiting attentional enhancement or weak suppression, whereas the SC exhibited predominantly attentional enhancement, which was significantly stronger than in the LGN. The spatial distribution of the attentional effects was unrelated to the retinotopic organization in either structure. The results demonstrate that each of the major subcortical visual pathways participates in attentional selection, and their differential magnitudes of modulation suggest distinct roles.

Does Attention Alter Appearance

Abrupt onsets in the visual field can change the appearance of subsequent stimuli, according to one interpretation, by engaging an attentional mechanism that increases effective stimulus contrast. However, abrupt onsets can also engage capacity-unlimited and thus attention-independent sensory mechanisms. We conducted a series of experiments to differentiate the sensory and attentional accounts. Observers compared the contrasts of uncued low-contrast peripheral targets with simultaneous targets cued by one of three cue types with different sensory attributes: white or black peripheral abrupt onsets and central gaze direction cues devoid of sensory activity near the target locations. Each cue facilitated the perception of perithreshold targets; however, the white abrupt onsets increased the perceived contrast of suprathreshold targets, whereas the black abrupt onsets tended to reduce the perceived contrast, and the gaze direction cues had no significant effect. The effectiveness of the gaze direction cues in automatically orienting attention was demonstrated in a control experiment in which they consistently speeded response times. The results suggest that sensory interaction, and not attention, is responsible for changes in appearance.

Subcortical Mechanisms of Feature-Based Attention

The degree to which spatial and feature-based attention are governed by similar control mechanisms is not clear. To explore this issue, I measured, during conditions of spatial or feature-based attention, activity in the human subcortical visual nuclei, which have precise retinotopic maps and are known to play important roles in the regulation of spatial attention but have limited selectivity of nonspatial features. Subjects attended to and detected changes in separate fields of moving or colored dots. When the fields were disjoint, spatially attending to one field enhanced hemodynamic responses in the superior colliculus (SC), lateral geniculate nucleus (LGN), and two retinotopic pulvinar nuclei. When the two dot fields were spatially overlapping, feature-based attention to the moving versus colored dots enhanced responses in the pulvinar nuclei and the majority of the LGN, including the magnocellular layers, and suppressed activity in some areas within the parvocellular layers; the SC was inconsistently modulated among subjects. The results demonstrate that feature-based attention operates throughout the visual system by prioritizing neurons encoding the attended information, including broadly tuned thalamic neurons. I conclude that spatial and feature-based attention operate via a common principle, but that spatial location is a special feature in that it is widely encoded in the brain, is used for overt orienting, and uses a specialized structure, the SC.

Attention alters decision criteria but not appearance: A reanalysis of Anton-Erxleben, Abrams, and Carrasco (2010)

Paying attention to a stimulus affords it many behavioral advantages, but whether attention also changes its subjective appearance is controversial. K. A. Schneider and M. Komlos (2008) demonstrated that the results of previous studies suggesting that attention increased perceived contrast could also be explained by a biased decision mechanism. This bias could be neutralized by altering the methodology to ask subjects whether two stimuli were equal in contrast or not rather than which had the higher contrast. K. Anton-Erxleben, J. Abrams, and M. Carrasco (2010) claimed that, even using this equality judgment, attention could still be shown to increase perceived contrast. In this reply, we analyze their data and conclude that the effects that they reported resulted from fitting symmetric functions that poorly characterized the individual subject data, which exhibited significant asymmetries between the high- and low-contrast tails. The strength of the effect attributed to attentional enhancement in each subject was strongly correlated with this skew. By refitting the data with a response model that included a non-zero asymptotic response in the low-contrast regime, we show that the reported attentional effects are better explained as changes in subjective criteria. Thus, the conclusion of Schneider and Komlos that attention biases the decision mechanism but does not alter appearance is still valid and is in fact supported by the data from Anton-Erxleben et al.

Reflexive gaze orienting induces the line-motion illusion

When a static line is presented near a brief cue, participants report motion within the line from the cued end towards the uncued end. Attention may mediate this effect by speeding the processing of the attended end of the line; however, apparent motion mechanisms between the cue and the line may also contribute. This study uses a new type of attentional cue, reflexive gaze orienting (RGO), which recruits attention automatically but uses a cue presented remotely from the line. Thus, RGO rules out motion mechanisms that might be recruited by a cue appearing in the vicinity of the line, and allows one to evaluate the contribution of attention per se to the illusion. In three experiments, RGO induced the line-motion illusion, establishing attention as a source of the illusion. Although attention may accelerate processing at the attended location, alternative mechanisms by which attention could cause the line-motion illusion are considered.

Morphological differences in the lateral geniculate nucleus associated with dyslexia

Developmental dyslexia is a common learning disability characterized by normal intelligence but difficulty in skills associated with reading, writing and spelling. One of the most prominent, albeit controversial, theories of dyslexia is the magnocellular theory, which suggests that malfunction of the magnocellular system in the brain is responsible for the behavioral deficits. We sought to test the basis of this theory by directly measuring the lateral geniculate nucleus (LGN), the only location in the brain where the magnocellular and parvocellular streams are spatially disjoint. Using high-resolution proton-density weighted MRI scans, we precisely measured the anatomical boundaries of the LGN in 13 subjects with dyslexia (five female) and 13 controls (three female), all 22–26 years old. The left LGN was significantly smaller in volume in subjects with dyslexia and also differed in shape; no differences were observed in the right LGN. The functional significance of this asymmetry is unknown, but these results are consistent with the magnocellular theory and support theories of dyslexia that involve differences in the early visual system.

Altered anterior visual system development following early monocular enucleation

Purpose Retinoblastoma is a rare eye cancer that generally occurs before 5 years of age and often results in enucleation (surgical removal) of the cancerous eye. In the present study, we sought to determine the consequences of early monocular enucleation on the morphological development of the anterior visual pathway including the optic chiasm and lateral geniculate nucleus. Methods A group of adults who had one eye enucleated early in life due to retinoblastoma was compared to binocularly intact controls. Although structural changes have previously been reported in late enucleation, we also collected data from one late enucleated participant to compare to our early enucleated participants. Measurements of the optic nerves, optic chiasm, optic tracts and lateral geniculate nuclei were evaluated from T1 weighted and proton density weighted images collected from each participant. Results The early monocular enucleation group exhibited overall degeneration of the anterior visual system compared to controls. Surprisingly, however, optic tract diameter and geniculate volume decreases were less severe contralateral to the remaining eye. Consistent with previous research, the late enucleated participant showed no asymmetry and significantly larger volume decreases in both geniculate nuclei compared to controls. Conclusions The novel finding of an asymmetry in morphology of the anterior visual system following long-term survival from early monocular enucleation indicates altered postnatal visual development. Possible mechanisms behind this altered development include recruitment of deafferented cells by crossing nasal fibres and/or geniculate cell retention via feedback from primary visual cortex. These data highlight the importance of balanced binocular input during postnatal maturation for typical anterior visual system morphology.

Population Receptive Field Estimation Reveals New Retinotopic Maps in Human Subcortex

The human subcortex contains multiple nuclei that govern the transmission of information to and among cortical areas. In the visual domain, these nuclei are organized into retinotopic maps. Because of their small size, these maps have been difficult to precisely measure using phase-encoded functional magnetic resonance imaging, particularly in the eccentricity dimension. Using instead the population receptive field model to estimate the response properties of individual voxels, we were able to resolve two previously unreported retinotopic maps in the thalamic reticular nucleus and the substantia nigra. We measured both the polar angle and eccentricity components, receptive field size and hemodynamic response function delay, in the these nuclei and in the lateral geniculate nucleus, the superior colliculus, and the lateral and intergeniculate pulvinars. The anatomical boundaries of these nuclei were delineated using multiple averaged proton density-weighted images and were used to constrain and confirm the functional activations. Deriving the retinotopic organization of these small, subcortical nuclei is the first step in exploring their response properties and their roles in neural dynamics.

Abnormal Lateral Geniculate Nucleus and Optic Chiasm in Human Albinism

Our objective was to measure how the misrouting of retinal ganglion cell (RGC) fibers affects the organization of the optic chiasm and lateral geniculate nuclei (LGN) in human albinism. We compared the chiasmal structures and the LGN in both pigmented controls and patients with albinism by using high‐resolution structural magnetic resonance imaging (MRI). We studied 12 patients with oculocutaneous albinism and 12 age‐matched pigmented controls. Using a 3T MRI scanner, we acquired a T1‐weighted three‐dimensional magnetization‐prepared rapid gradient‐echo (MPRAGE) image of the whole brain, oriented so that the optic nerves, chiasm, and tracts were in the same plane. We acquired multiple proton density‐weighted images centered on the thalamus and midbrain, and averaged them to increase the signal, enabling precise manual tracing of the anatomical boundaries of the LGN. Albinism patients exhibited significantly smaller diameters of the optic nerves, chiasm and tracts, and optic chiasm and LGN volume compared with controls (P < 0.001 for all). The reductions in chiasmal diameters in the albinism compared with the control group can be attributed to the abnormal crossing of optic fibers and the reduction of RGCs in the central retina. The volume of the LGN devoted to the center of the visual field may be reduced in albinism due to fewer RGCs representing the area where the fovea would normally lie. Our data may be clinically useful in addressing how genetic deficits compromise proper structural and functional development in the brain. J. Comp. Neurol. 522:2680–2687, 2014.