A three-response task reveals how attention alters decision criteria but not appearance.

Whether attention alters appearance or just changes decision criteria continues to be controversial. When subjects are forced to choose which of two equal targets, one of which has been pre-cued, has a higher contrast, they tend to choose the cued target. This has been interpreted as attention increasing the apparent contrast of the cued target. However, when subjects must decide whether the two targets have equal or unequal contrast, they respond veridically with no apparent effect of attention. The discrepancy between these comparative and equality judgments is explained by attention altering the decision criteria but not appearance. We supposed that when subjects are forced to choose which of two apparently equal targets has the higher contrast, they tend to proportion their uncertainty in favor of the cued target. To test this hypothesis, we used a three-response task, in which subjects chose which target had the higher contrast but also had the option to report that the targets appeared equal. This task disentangled potential attention effects on appearance from those on the decision criteria. We found that subjects with narrower criteria about what constituted equal contrast were more likely to choose the cued target, supporting the uncertainty stealing hypothesis. Across the population, the effects of the attentional cue are explained as changes in the decision criteria and not changes in appearance.

Larger Auditory Cortical Area and Broader Frequency Tuning Underlie Absolute Pitch.

Absolute pitch (AP), the ability of some musicians to precisely identify and name musical tones in isolation, is associated with a number of gross morphological changes in the brain, but the fundamental neural mechanisms underlying this ability have not been clear. We presented a series of logarithmic frequency sweeps to age- and sex-matched groups of musicians with or without AP and controls without musical training. We used fMRI and population receptive field (pRF) modeling to measure the responses in the auditory cortex in 61 human subjects. The tuning response of each fMRI voxel was characterized as Gaussian, with independent center frequency and bandwidth parameters. We identified three distinct tonotopic maps, corresponding to primary (A1), rostral (R), and rostral-temporal (RT) regions of auditory cortex. We initially hypothesized that AP abilities might manifest in sharper tuning in the auditory cortex. However, we observed that AP subjects had larger cortical area, with the increased area primarily devoted to broader frequency tuning. We observed anatomically that A1, R and RT were significantly larger in AP musicians than in non-AP musicians or control subjects, which did not differ significantly from each other. The increased cortical area in AP in areas A1 and R were primarily low frequency and broadly tuned, whereas the distribution of responses in area RT did not differ significantly. We conclude that AP abilities are associated with increased early auditory cortical area devoted to broad-frequency tuning and likely exploit increased ensemble encoding.SIGNIFICANCE STATEMENT Absolute pitch (AP), the ability of some musicians to precisely identify and name musical tones in isolation, is associated with a number of gross morphological changes in the brain, but the fundamental neural mechanisms have not been clear. Our study shows that AP musicians have significantly larger volume in early auditory cortex than non-AP musicians and non-musician controls and that this increased volume is primarily devoted to broad-frequency tuning. We conclude that AP musicians are likely able to exploit increased ensemble representations to encode and identify frequency.

Hemispheric asymmetries in the orientation and location of the lateral geniculate nucleus in dyslexia.

Human brain asymmetry reflects normal specialization of functional roles and may derive from evolutionary, hereditary, developmental, experiential, and pathological factors (Toga & Thompson, 2003). Geschwind and Galaburda (1985) suggested that processing difficulties in dyslexia are due to structural differences between hemispheres. Because of its potential significance to the controversial magnocellular theory of dyslexia, we investigated hemispheric differences in the human lateral geniculate nucleus (LGN), the primary visual relay and control nucleus in the thalamus, in subjects with dyslexia compared to normal readers. We acquired and averaged multiple high-resolution proton density (PD) weighted structural magnetic resonance imaging (MRI) volumes to measure in detail the anatomical boundaries of the LGN in each hemisphere. We observed hemispheric asymmetries in the orientation of the nucleus in subjects with dyslexia that were absent in controls. We also found differences in the location of the LGN between hemispheres in controls but not in subjects with dyslexia. Neither the precise anatomical differences in the LGN nor their functional consequences are known, nor is it clear whether the differences might be causes or effects of dyslexia.

Interhemispheric interactions of the human thalamic reticular nucleus.

The thalamic reticular nucleus is an important structure governing the recurrent interactions between the thalamus and cortex that may provide a substrate for unified perception. Despite the importance of the TRN, its activity has been scarcely investigated in vivo in animal models, and never in humans. Here we anatomically identify the human TRN using multiple registered and averaged proton density-weighted structural MRI scans and drive its functional activity with a dual phase-encoded stimulus. We characterize the retinotopic and temporal response properties in the visual sector of the TRN and measured an inhibitory relationship with the contralateral LGN. These observations provide a basis for further gross characterizations of the role of the TRN in human behavior.

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.

Neural Dynamics during Binocular Rivalry: Indications from Human Lateral Geniculate Nucleus.

When two sufficiently different stimuli are presented to each eye, perception alternates between them. This binocular rivalry is conceived as a competition for representation in the single stream of visual consciousness. The magnocellular (M) and parvocellular (P) pathways, originating in the retina, encode disparate information, but their potentially different contributions to binocular rivalry have not been determined. Here, we used functional magnetic resonance imaging to measure the human lateral geniculate nucleus (LGN), where the M and P neurons are segregated into layers receiving input from a single eye. We had three participants (one male, two females) and used achromatic stimuli to avoid contributions from color opponent neurons that may have confounded previous studies. We observed activity in the eye-specific regions of LGN correlated with perception, with similar magnitudes during rivalry or physical stimuli alternations, also similar in the M and P regions. These results suggest that LGN activity reflects our perceptions during binocular rivalry and is not simply an artifact of color opponency. Further, perception appears to be a global phenomenon in the LGN, not just limited to a single information channel.

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.

A specialized channel for encoding auditory transients in the magnocellular division of the human medial geniculate nucleus.

We test the hypothesis that there exists a generalized magnocellular system in the brain optimized for temporal processing. In the visual system, it is well known that the magnocellular layers in the lateral geniculate nucleus (LGN) are strongly activated by transients and quickly habituate. However, little is known about the perhaps analogous magnocellular division of the medial geniculate nucleus (MGN), the auditory relay in the thalamus. We measured the functional responses of the MGN in 11 subjects who passively listened to sustained and transient nonlinguistic sounds, using functional MRI. We observed that voxels in the ventromedial portion of the MGN, corresponding to the magnocellular division, exhibited a robust preference to transient sounds, consistently across subjects, whereas the remainder of the MGN did not discriminate between sustained and transient sounds. We conclude that the magnocellular neurons in the MGN parallel the magnocellular neurons in its visual counterpart, LGN, and constitute an information stream specialized for encoding auditory dynamics.

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.

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.

Neural correlates of binocular rivalry in the human lateral geniculate nucleus.

When dissimilar images are presented to the two eyes, they compete for perceptual dominance so that only one image is visible at a time while the other one is suppressed. Neural correlates of such binocular rivalry have been found at multiple stages of visual processing, including striate and extrastriate visual cortex. However, little is known about the role of subcortical processing during binocular rivalry. Here we used fMRI to measure neural activity in the human LGN while subjects viewed contrast-modulated gratings presented dichoptically. Neural activity in the LGN correlated strongly with the subjects' reported percepts, such that activity increased when a high-contrast grating was perceived and decreased when a low-contrast grating was perceived. Our results provide evidence for a functional role of the LGN in binocular rivalry and suggest that the LGN, traditionally viewed as the gateway to the visual cortex, may be an early gatekeeper of visual awareness.

Distinguishing Hemodynamics from Function in the Human LGN Using a Temporal Response Model.

We developed a temporal population receptive field model to differentiate the neural and hemodynamic response functions (HRF) in the human lateral geniculate nucleus (LGN). The HRF in the human LGN is dominated by the richly vascularized hilum, a structure that serves as a point of entry for blood vessels entering the LGN and supplying the substrates of central vision. The location of the hilum along the ventral surface of the LGN and the resulting gradient in the amplitude of the HRF across the extent of the LGN have made it difficult to segment the human LGN into its more interesting magnocellular and parvocellular regions that represent two distinct visual processing streams. Here, we show that an intrinsic clustering of the LGN responses to a variety of visual inputs reveals the hilum, and further, that this clustering is dominated by the amplitude of the HRF. We introduced a temporal population receptive field model that includes separate sustained and transient temporal impulse response functions that vary on a much short timescale than the HRF. When we account for the HRF amplitude, we demonstrate that this temporal response model is able to functionally segregate the residual responses according to their temporal properties.

Attention biases decisions but does not alter appearance.

Recently, M. Carrasco, S. Ling, and S. Read (2004) reported that transient visual attentional cues could increase the perceived contrast of Gabor grating targets. We replicated their study using their exact stimuli and procedures. While we were able to reproduce their results, we discovered that the reported attentional effects vanished when we changed the type of decision that subjects performed from a comparative judgment ("which target has higher contrast?") to an equality judgment ("are the two targets equal in contrast?") that is resistant to bias. To ensure that the difference between the judgments was not due to a difference in attentional strategies, we also performed a control experiment in which subjects were instructed on a trial-by-trial basis which judgment to perform only after the stimuli had disappeared. In this experiment, the magnitude of attentional effect for the comparative judgment was diminished but still significant and the equality judgment still measured no effect. We conclude that the reported effects of attention upon appearance can be entirely explained by decision bias, and that attention does not alter appearance.

The Flash-Lag, Fröhlich and Related Motion Illusions Are Natural Consequences of Discrete Sampling in the Visual System.

The Fröhlich effect and flash-lag effect, in which moving objects appear advanced along their trajectories compared to their actual positions, have defied a simple and consistent explanation. Here, I show that these illusions can be understood as a natural consequence of temporal compression in the human visual system. Discrete sampling at some stage of sensory perception has long been considered, and if it were true, it would necessarily lead to these illusions of motion. I show that the discrete perception hypothesis, with a single free parameter, the perceptual moment or sampling rate, can quantitatively explain all of the scenarios of the Fröhlich and flash-lag effect. I interpret discrete perception as the implementation of data compression in the brain, and our conscious perception as the reconstruction of the compressed input.

Beyond a relay nucleus: neuroimaging views on the human LGN.

The lateral geniculate nucleus (LGN) is the thalamic station in the retinocortical projection and has traditionally been viewed as the gateway for sensory information to enter the cortex. Here, we review recent studies of the human LGN that have investigated the retinotopic organization, physiologic response properties, and modulation of neural activity by selective attention and by visual awareness in a binocular rivalry paradigm. In the retinotopy studies, we found that the contralateral visual field was represented with the lower field in the medial-superior portion and the upper field in the lateral-inferior portion of each LGN. The fovea was represented in posterior and superior portions, with increasing eccentricities represented more anteriorly. Functional MRI responses increased monotonically with stimulus contrast in the LGN and in visual cortical areas. In the LGN, the dynamic response range of the contrast function was larger and contrast gain was lower than in the cortex. In our attention studies, we found that directed attention to a spatial location modulated neural activity in the LGN in several ways: it enhanced neural responses to attended stimuli, attenuated responses to ignored stimuli, and increased baseline activity in the absence of visual stimulation. Furthermore, we showed in a binocular rivalry paradigm that neural activity in the LGN correlated strongly with the subjects' reported percepts. The overall view that emerges from these studies is that the human LGN plays a role in perception and cognition far beyond that of a relay nucleus and, rather, needs to be considered as an early gatekeeper in the control of visual attention and awareness.

Measuring Connectivity in the Primary Visual Pathway in Human Albinism Using Diffusion Tensor Imaging and Tractography.

In albinism, the number of ipsilaterally projecting retinal ganglion cells (RGCs) is significantly reduced. The retina and optic chiasm have been proposed as candidate sites for misrouting. Since a correlation between the number of lateral geniculate nucleus (LGN) relay neurons and LGN size has been shown, and based on previously reported reductions in LGN volumes in human albinism, we suggest that fiber projections from LGN to the primary visual cortex (V1) are also reduced. Studying structural differences in the visual system of albinism can improve the understanding of the mechanism of misrouting and subsequent clinical applications. Diffusion data and tractography are useful for mapping the OR (optic radiation). This manuscript describes two algorithms for OR reconstruction in order to compare brain connectivity in albinism and controls.An MRI scanner with a 32-channel head coil was used to acquire structural scans. A T1-weighted 3D-MPRAGE sequence with 1 mm(3) isotropic voxel size was used to generate high-resolution images for V1 segmentation. Multiple proton density (PD) weighted images were acquired coronally for right and left LGN localization. Diffusion tensor imaging (DTI) scans were acquired with 64 diffusion directions. Both deterministic and probabilistic tracking methods were run and compared, with LGN as the seed mask and V1 as the target mask. Though DTI provides relatively poor spatial resolution, and accurate delineation of OR may be challenging due to its low fiber density, tractography has been shown to be advantageous both in research and clinically. Tract based spatial statistics (TBSS) revealed areas of significantly reduced white matter integrity within the OR in patients with albinism compared to controls. Pairwise comparisons revealed a significant reduction in LGN to V1 connectivity in albinism compared to controls. Comparing both tracking algorithms revealed common findings, strengthening the reliability of the technique.

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 x 1.5 x 2 mm3) at 3 tesla to investigate the retinotopic organization of the human lateral geniculate nucleus (LGN). The central 15 degrees 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.

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.

High-resolution Structural Magnetic Resonance Imaging of the Human Subcortex In Vivo and Postmortem.

The focus of this study was to test the resolution limits of structural MRI of a postmortem brain compared to living human brains. The resolution of structural MRI in vivo is ultimately limited by physiological noise, including pulsation, respiration and head movement. Although imaging hardware continues to improve, it is still difficult to resolve structures on the millimeter scale. For example, the primary visual sensory pathways synapse at the lateral geniculate nucleus (LGN), a visual relay and control nucleus in the thalamus that normally is organized into six interleaved monocular layers. Neuroimaging studies have not been able to reliably distinguish these layers due their small size that are less than 1 mm thick. The resolving limit of structural MRI, in a postmortem brain was tested using multiple images averaged over a long duration (~24 h). The purpose was to test whether it was possible to resolve the individual layers of the LGN in the absence of physiological noise. A proton density (PD)(1) weighted pulse sequence was used with varying resolution and other parameters to determine the minimum number of images necessary to be registered and averaged to reliably distinguish the LGN and other subcortical regions. The results were also compared to images acquired in living human brains. In vivo subjects were scanned in order to determine the additional effects of physiological noise on the minimum number of PD scans needed to differentiate subcortical structures, useful in clinical applications.

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.