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This page is a list of articles suggested for Vision Lunch.

Please feel free to add any interesting articles to this list.

Local Visual Energy Mechanisms Revealed by Detection of Global Patterns Yaniv Morgenstern and James H. Elder

A central goal of visual neuroscience is to relate the selectivity of individual neurons to perceptual judgments, such as detection of a visual pattern at low contrast or in noise. Since neurons in early areas of visual cortex carry information only about a local patch of the image, detection of global patterns must entail spatial pooling over many such neurons. Physiological methods provide access to local detection mechanisms at the single-neuron level but do not reveal how neural responses are combined to determine the perceptual decision. Behavioral methods provide access to perceptual judgments of a global stimulus but typically do not reveal the selectivity of the individual neurons underlying detection. Here we show how the existence of a nonlinearity in spatial pooling does allow properties of these early mechanisms to be estimated from behavioral responses to global stimuli. As an example, we consider detection of large-field sinusoidal gratings in noise. Based on human behavioral data, we estimate the length and width tuning of the local detection mechanisms and show that it is roughly consistent with the tuning of individual neurons in primary visual cortex of primate. We also show that a local energy model of pooling based on these estimated receptive fields is much more predictive of human judgments than competing models, such as probability summation. In addition to revealing underlying properties of early detection and spatial integration mechanisms in human cortex, our findings open a window on new methods for relating system-level perceptual judgments to neuron-level processing.

Timing, Timing, Timing: Fast Decoding of Object Information from Intracranial Field Potentials in Human Visual Cortex Hesheng Liu1,2,Yigal Agam1,Joseph R. Madsen3andGabriel Kreiman

The difficulty of visual recognition stems from the need to achieve high selectivity while maintaining robustness to object transformations within hundreds of milliseconds. Theories of visual recognition differ in whether the neuronal circuits invoke recurrent feedback connections or not. The timing of neurophysiological responses in visual cortex plays a key role in distinguishing between bottom-up and top-down theories. Here, we quantified at millisecond resolution the amount of visual information conveyed by intracranial field potentials from 912 electrodes in 11 human subjects. We could decode object category information from human visual cortex in single trials as early as 100 ms poststimulus. Decoding performance wasrobust to depth rotation and scale changes. The results suggest that physiological activity in thetemporal lobe can account for key properties of visual recognition. The fast decoding in single trials is compatible with feedforward theories and provides strong constraints for computational models of human vision.

Comparing face patch systems in macaques and humans.

Tsao DY, Moeller S, Freiwald WA.

Face recognition is of central importance for primate social behavior. In both humans and macaques, the visual analysis of faces is supported by a set of specialized face areas. The precise organization of these areas and the correspondence between individual macaque and human face-selective areas are debated. Here, we examined the organization of face-selective regions across the temporal lobe in a large number of macaque and human subjects. Macaques showed 6 regions of face-selective cortex arranged in a stereotypical pattern along the temporal lobe. Human subjects showed, in addition to 3 reported face areas (the occipital, fusiform, and superior temporal sulcus face areas), a face-selective area located anterior to the fusiform face area, in the anterior collateral sulcus. These results suggest a closer anatomical correspondence between macaque and human face-processing systems than previously realized.

Suggested by Davie

'Anatomical Evidence for Classical and Extra-classical Receptive Field Completion Across the Discontinuous Horizontal Meridian Representation of Primate Area V2'

Jeffs J, Ichida JM, Federer F, Angelucci A

Cereb Cortex. 2008 Sep 16

In primates, a split of the horizontal meridian (HM) representation at the V2 rostral border divides this area into dorsal (V2d) and ventral (V2v) halves (representing lower and upper visual quadrants, respectively), causing retinotopically neighboring loci across the HM to be distant within V2. How is perceptual continuity maintained across this discontinuous HM representation? Injections of neuroanatomical tracers in marmoset V2d demonstrated that cells near the V2d rostral border can maintain retinotopic continuity within their classical and extra-classical receptive field (RF), by making both local and long-range intra- and interareal connections with ventral cortex representing the upper visual quadrant. V2d neurons located <0.9-1.3 mm from the V2d rostral border, whose RFs presumably do not cross the HM, make nonretinotopic horizontal connections with V2v neurons in the supra- and infragranular layers. V2d neurons located <0.6-0.9 mm from the border, whose RFs presumably cross the HM, in addition make retinotopic local connections with V2v neurons in layer 4. V2d neurons also make interareal connections with upper visual field regions of extrastriate cortex, but not of MT or MTc outside the foveal representation. Labeled connections in ventral cortex appear to represent the "missing" portion of the connectional fields in V2d across the HM. We conclude that connections between dorsal and ventral cortex can create visual field continuity within a second-order discontinuous visual topography.

Suggested by Davie, mentioned by this week's Wandell lab speaker

Dynamic Population Coding of Category Information in Inferior Temporal and Prefrontal Cortex

Ethan M. Meyers, David J. Freedman, Gabriel Kreiman, Earl K. Miller and Tomaso Poggio

Journal of Neurophysiology 100: 1407-1419, 2008

Most electrophysiology studies analyze the activity of each neuron separately. While such studies have given much insight into properties of the visual system, they have also potentially overlooked important aspects of information coded in changing patterns of activity that are distributed over larger populations of neurons. In this work, we apply a population decoding method to better estimate what information is available in neuronal ensembles and how this information is coded in dynamic patterns of neural activity in data recorded from inferior temporal cortex (ITC) and prefrontal cortex (PFC) as macaque monkeys engaged in a delayed match-to-category task. Analyses of activity patterns in ITC and PFC revealed that both areas contain "abstract" category information (i.e., category information that is not directly correlated with properties of the stimuli); however, in general, PFC has more task-relevant information, and ITC has more detailed visual information. Analyses examining how information coded in these areas show that almost all category information is available in a small fraction of the neurons in the population. Most remarkably, our results also show that category information is coded by a nonstationary pattern of activity that changes over the course of a trial with individual neurons containing information on much shorter time scales than the population as a whole.

  • Suggested by Sayres 12:38, 30 September 2008 (PDT)

Visual long-term memory has a massive storage capacity for object details
Timothy F. Brady*, Talia Konkle, George A. Alvarez, and Aude Oliva* [link]

One of the major lessons of memory research has been that human memory is fallible, imprecise, and subject to interference. Thus, although observers can remember thousands of images, it is widely assumed that these memories lack detail. Contrary to this assumption, here we show that long-term memory is capable of storing a massive number of objects with details from the image. Participants viewed pictures of 2,500 objects over the course of 5.5 h. Afterward, they were shown pairs of images and indicated which of the two they had seen. The previously viewed item could be paired with either an object from a novel category, an object of the same basic-level category, or the same object in a different state or pose. Performance in each of these conditions was remarkably high (92%, 88%, and 87%, respectively), suggesting that participants successfully maintained detailed representations of thousands of images. These results have implications for cognitive models, in which capacity limitations impose a primary computational constraint (e.g., models of object recognition), and pose a challenge to neural models of memory storage and retrieval, which must be able to account for such a large and detailed storage capacity.

Suggested by Davie, possible joint meeting with Wagner lab?

Spatio-temporal correlations and visual signalling in a complete neuronal population
Pillow JW, Shlens J, Paninski L, Sher A, Litke AM, Chichilnisky EJ, Simoncelli EP. [link]

Statistical dependencies in the responses of sensory neurons govern both the amount of stimulus information conveyed and the means by which downstream neurons can extract it. Although a variety of measurements indicate the existence of such dependencies, their origin and importance for neural coding are poorly understood. Here we analyse the functional significance of correlated firing in a complete population of macaque parasol retinal ganglion cells using a model of multi-neuron spike responses. The model, with parameters fit directly to physiological data, simultaneously captures both the stimulus dependence and detailed spatio-temporal correlations in population responses, and provides two insights into the structure of the neural code. First, neural encoding at the population level is less noisy than one would expect from the variability of individual neurons: spike times are more precise, and can be predicted more accurately when the spiking of neighbouring neurons is taken into account. Second, correlations provide additional sensory information: optimal, model-based decoding that exploits the response correlation structure extracts 20% more information about the visual scene than decoding under the assumption of independence, and preserves 40% more visual information than optimal linear decoding. This model-based approach reveals the role of correlated activity in the retinal coding of visual stimuli, and provides a general framework for understanding the importance of correlated activity in populations of neurons.

Suggested by Davie

Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex
Leeland B. Ekstrom,1,2,3 Pieter R. Roelfsema,4,5 John T. Arsenault,1,6 Giorgio Bonmassar,1 Wim Vanduffel1,6,7* [link]

The frontal eye field (FEF) is one of several cortical regions thought to modulate sensory inputs. Moreover, several hypotheses suggest that the FEF can only modulate early visual areas in the presence of a visual stimulus. To test for bottom-up gating of frontal signals, we microstimulated subregions in the FEF of two monkeys and measured the effects throughout the brain with functional magnetic resonance imaging. The activity of higher-order visual areas was strongly modulated by FEF stimulation, independent of visual stimulation. In contrast, FEF stimulation induced a topographically specific pattern of enhancement and suppression in early visual areas, but only in the presence of a visual stimulus. Modulation strength depended on stimulus contrast and on the presence of distractors. We conclude that bottom-up activation is needed to enable top-down modulation of early visual cortex and that stimulus saliency determines the strength of this modulation.

Suggested by Davie -- possible joint with Moore/Newsome labs? Maybe Nathan is on top of this already.

A Stable Topography of Selectivity for Unfamiliar Shape Classes in Monkey Inferior Temporal Cortex Hans P. Op de Beeck, Jennifer A. Deutsch, Wim Vanduffel, Nancy G. Kanwisher, and James J. DiCarlo Cerebral Cortex Advance Access published on November 21, 2007 Cereb. Cortex 2008 18: 1676-1694; doi:10.1093/cercor/bhm196

The inferior temporal (IT) cortex in monkeys plays a central role in visual object recognition and learning. Previous studies have observed patches in IT cortex with strong selectivity for highly familiar objectclasses (e.g., faces), but the principles behind this functional organization are largely unknown due to the many properties that distinguish different object classes. To unconfound shape from meaning and memory, we scanned monkeys with functional magnetic resonance imaging while they viewed classes of initially novel objects. Our data revealed a topography of selectivity for these novel object classes across IT cortex. We found that this selectivity topography was highly reproducible and remarkably stable across a 3-month interval during which monkeys were extensively trained to discriminate among exemplars within one of the object classes. Furthermore, this selectivity topography was largely unaffected by changes in behavioral task and object retinal position, both of which preserve shape. In contrast, it was strongly influenced by changes in object shape. The topography was partially related to, but not explained by, the previously described pattern of face selectivity. Together, these results suggest that IT cortex contains a large-scale map of shape that is largely independent of meaning, familiarity, and behavioral task.
Suggested by Kaoru

Treating congenital blindness in dogs and humans

Aguirre et al, PLoS Medicine 2007

RPE65 is an essential molecule in the retinoid-visual cycle, and RPE65 gene mutations cause the congenital human blindness known as Leber congenital amaurosis (LCA). Somatic gene therapy delivered to the retina of blind dogs with an RPE65 mutation dramatically restores retinal physiology and has sparked international interest in human treatment trials for this incurable disease. An unanswered question is how the visual cortex responds after prolonged sensory deprivation from retinal dysfunction. We therefore studied the cortex of RPE65-mutant dogs before and after retinal gene therapy. Then, we inquired whether there is visual pathway integrity and responsivity in adult humans with LCA due to RPE65 mutations (RPE65-LCA). Sayres 12:35, 25 June 2008 (PDT)

Tuned Responses of Astrocytes and Their Influence on Hemodynamic Signals in the Visual Cortex

James Schummers, Hongbo Yu, Mriganka Sur (in Science)

Astrocytes have long been thought to act as a support network for neurons, with little role in information representation or processing. We used two-photon imaging of calcium signals in the ferret visual cortex in vivo to discover that astrocytes, like neurons, respond to visual stimuli, with distinct spatial receptive fields and sharp tuning to visual stimulus features including orientation and spatial frequency. The stimulus-feature preferences of astrocytes were exquisitely mapped across the cortical surface, in close register with neuronal maps. The spatially restricted stimulus-specific component of the intrinsic hemodynamic mapping signal was highly sensitive to astrocyte activation, indicating that astrocytes have a key role in coupling neuronal organization to mapping signals critical for noninvasive brain imaging. Furthermore, blocking astrocyte glutamate transporters influenced the magnitude and duration of adjacent visually driven neuronal responses. --Bob 09:55, 20 June 2008 (PDT)

The effects of priming on frontal-temporal communication
Avniel S. Ghuman, Moshe Bar, Ian G. Dobbins, and David M. Schnyer PDF
Repeated exposure to a stimulus facilitates its processing. This is reflected in faster and more accurate identification, reduced perceptual identification thresholds, and more efficient classifications for repeated compared with novel items. Here, we test a hypothesis that this experience-based behavioral facilitation is a result of enhanced communication between distinct cortical regions, which reduces local processing demands. A magnetoencephalographic investigation revealed that repeated object classification led to decreased neural responses in the prefrontal cortex and temporal cortex. Critically, this decrease in absolute activity was accompanied by greater neural synchrony (a measure of functional connectivity) between these regions with repetition. Additionally, the onset of the enhanced interregional synchrony predicted the degree of behavioral facilitation. These findings suggest that object repetition results in enhanced interactions between brain regions, which facilitates performance and reduces processing demands on the regions involved. Suggested by Davie

Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues
Li W, Howard JD, Parrish TB, Gottfried JA

Learning to associate sensory cues with threats is critical for minimizing aversive experience. The ecological benefit of associative learning relies on accurate perception of predictive cues, but how aversive learning enhances perceptual acuity of sensory signals, particularly in humans, is unclear. We combined multivariate functional magnetic resonance imaging with olfactory psychophysics to show that initially indistinguishable odor enantiomers (mirror-image molecules) become discriminable after aversive conditioning, paralleling the spatial divergence of ensemble activity patterns in primary olfactory (piriform) cortex. Our findings indicate that aversive learning induces piriform plasticity with corresponding gains in odor enantiomer discrimination, underscoring the capacity of fear conditioning to update perceptual representation of predictive cues, over and above its well-recognized role in the acquisition of conditioned responses. That completely indiscriminable sensations can be transformed into discriminable percepts further accentuates the potency of associative learning to enhance sensory cue perception and support adaptive behavior. Suggested by Davie

Peripheral variability and central constancy in mammalian visual system evolution
Kaskan PM, Franco EC, Yamada ES, Silveira LC, Darlington RB, Finlay BL. 2005. Proc. Biol. Sci

Neural systems are necessarily the adaptive products of natural selection, but a neural system, dedicated to any particular function in a complex brain, may be composed of components that covary with functionally unrelated systems, owing to constraints beyond immediate functional requirements. Some studies support a modular or mosaic organization of the brain, whereas others emphasize coordination and covariation. To contrast these views, we have analysed the retina, striate cortex (V1) and extrastriate cortex (V2, V3, MT, etc.) in 30 mammals, examining the area of the neocortex and individual neocortical areas and the relative numbers of rods and cones. Controlling for brain size and species relatedness, the sizes of visual cortical areas (striate, extrastriate) within the brains of nocturnal and diurnal mammals are not statistically different from one another. The relative sizes of all cortical areas, visual, somatosensory and auditory, are best predicted by the total size of the neocortex. In the sensory periphery, the retina is clearly specialized for niche. New data on rod and cone numbers in various New World primates confirm that rod and cone complements of the retina vary substantially between nocturnal and diurnal species. Although peripheral specializations or receptor surfaces may be highly susceptible to niche-specific selection pressures, the areal divisions of the cerebral cortex are considerably more conservative. Suggested by Davie

Ultra low field-strength MRI with simultaneous MEG Zotev et al, on arXiv

Abstract: Magnetic resonance imaging at ultra-low fields (ULF MRI) uses SQUIDs (superconducting quantum interference devices) to measure spin precession at a microtesla-range field after sample magnetization is enhanced by a stronger pre-polarizing field. Here, the first ULF images of the human head acquired at 46 microtesla measurement field with pre-polarization at 30 mT are reported. The imaging was performed with 3 mm x 3 mm x 6 mm resolution using the seven-channel SQUID system designed for both ULF MRI and magnetoencephalography (MEG). Auditory MEG signals were measured immediately after the imaging while the human subject remained inside the system. These results demonstrate that ULF MRI of the human brain is feasible and can be naturally combined with MEG.

This is a short conference paper (1 page!), but may serve as a nice jumping off point to discuss ultra low-field MRI, which has been around for over a decade.

Sayres 12:33, 10 November 2007 (PST)

Invariance and object representation

DiCarlo & Cox, TICS, 2007

Untangling invariant object recognition.

Despite tremendous variation in the appearance of visual objects, primates can recognize a multitude of objects, each in a fraction of a second, with no apparent effort. However, the brain mechanisms that enable this fundamental ability are not understood. Drawing on ideas from neurophysiology and computation, we present a graphical perspective on the key computational challenges of object recognition, and argue that the format of neuronal population representation and a property that we term 'object tangling' are central. We use this perspective to show that the primate ventral visual processing stream achieves a particularly effective solution in which single-neuron invariance is not the goal. Finally, we speculate on the key neuronal mechanisms that could enable this solution, which, if understood, would have far-reaching implications for cognitive neuroscience.

Suggested by KGS (?)

Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior.

Michael D. Fox Abraham Z. Snyder, Justin L. Vincent, and Marcus E. Raichle Neuron 2007

The resting brain is not silent, but exhibits organized fluctuations in neuronal activity even in the absence of tasks or stimuli. This intrinsic brain activity persists during task performance and contributes to variability in evoked brain responses. What is unknown is if this intrinsic activity also contributes to variability in behavior. In the current fMRI study, we identify a relationship between human brain activity in the left somatomotor cortex and spontaneous trial-to-trial variability in button press force. We then demonstrate that 74% of this brain-behavior relationship is attributable to ongoing fluctuations in intrinsic activity similar to those observed during resting fixation. In addition to establishing a functional and behavioral significance of intrinsic brain activity, these results lend new insight into the origins of variability in human behavior.

Suggested by Rory

Individual differences in white-matter microstructure reflect variation in functional connectivity during choice.

Paired-pulse transcranial magnetic stimulation indexed functional connectivity between two regions important for action choices: the premotor and motor cortex. Individual differences in functional connectivity during action selection show highly specific correlations with FA in localized regions of white-matter interconnecting regions, including the premotor and motor cortex. These findings demonstrate a relationship between individual differences in functional and structural connectivity within human brain networks central to action choice.

Boorman et al, 2007

Suggested by Davie (?)

Early visual deprivation impairs multisensory interactions in humans Lisa Putzar, Ines Goerendt, Kathrin Lange, Frank Ro¨sler & Brigitte Ro¨der; Nature Neuroscience 2007

Animal studies have shown that visual deprivation during the first months of life permanently impairs the interactions between sensory systems. Here we report an analogous effect for humans who had been deprived of pattern vision for at least the first five months of their life as a result of congenital binocular cataracts. These patients showed reduced audiovisual interactions in later life, although their visual performance in control tasks was unimpaired. Thus, adequate (multisensory) input during the first months of life seems to be a prerequisite in humans, as well as in animals, for the full development of cross-modal interactions.

[Roder, NN 2007]

Suggested by Michal

Robust detection of ocular dominance columns in humans using Hahn Spin Echo BOLD functional MRI at 7 Tesla.

Yacoub E, Shmuel A, Logothetis N, Uğurbil K. NeuroImage 2007

Cells in the mammalian brain tend to be grouped together according to their afferent and efferent connectivity, as well as their physiological properties. The columnar structures of neocortex are prominent examples of such modular organization, and have been studied extensively in anatomical and physiological experiments in rats, cats and monkeys. The importance of noninvasive study of such structures, in particular in human subjects, cannot be overemphasized. Not surprisingly, therefore, many attempts were made to map cortical columns using functional magnetic resonance imaging (fMRI). Yet, the robustness, repeatability, and generality of the hitherto used fMRI methodologies have been a subject of intensive debate. Using differential mapping in a high magnetic field magnet (7 T), we demonstrate here the ability of Hahn Spin-Echo (HSE) BOLD to map the ocular dominance columns (ODCs) of the human visual cortex reproducibly over several days with a high degree of accuracy, relative to expected spatial patterns from post-mortem data. On the other hand, the conventional Gradient-Echo (GE) blood oxygen level dependent (BOLD) signal in some cases failed to resolve ODCs uniformly across the selected gray matter region, due to the presence of non-specific signals. HSE signals uniformly resolved the ODC patterns, providing a more generalized mapping methodology (i.e. one that does not require adjusting experimental approaches based on prior knowledge or assumptions about functional organization and vascular structure in order to avoid confounding large vessel effects) to map unknown columnar systems in the human brain, potentially paving the way both for the study of the functional architecture of human sensory cortices, and of brain modules underlying specific cognitive processes.

Suggested by KGS. We should invite Gary over to read along with us.

Rapid and precise retinotopic mapping of the visual cortex obtained by voltage-sensitive dye imaging in the behaving monkey.

Yang Z, Heeger DJ, Seidemann E. J. Neurophysiology, 2007

Retinotopy is a fundamental organizing principle of the visual cortex. Over the years, a variety of techniques have been used to examine it. None of these techniques, however, provides a way to rapidly characterize retinotopy, at the submillimeter range, in alert, behaving subjects. Voltage-sensitive dye imaging (VSDI) can be used to monitor neuronal population activity at high spatial and temporal resolutions. Here we present a VSDI protocol for rapid and precise retinotopic mapping in the behaving monkey. Two monkeys performed a fixation task while thin visual stimuli swept periodically at a high speed in one of two possible directions through a small region of visual space. Because visual space is represented systematically across the cortical surface, each moving stimulus produced a traveling wave of activity in the cortex that could be precisely measured with VSDI. The time at which the peak of the traveling wave reached each location in the cortex linked this location with its retinotopic representation. We obtained detailed retinotopic maps from a region of about 1 cm(2) over the dorsal portion of areas V1 and V2. Retinotopy obtained during <4 min of imaging had a spatial precision of 0.11-0.19 mm, was consistent across experiments, and reliably predicted the locations of the response to small localized stimuli. The ability to rapidly obtain precise retinotopic maps in behaving monkeys opens the door for detailed analysis of the relationship between spatiotemporal dynamics of population responses in the visual cortex and perceptually guided behavior.

Suggested by Kevin and David

A temporal frequency–dependent functional architecture in human V1 revealed by high-resolution fMRI

Pei Sun1, Kenichi Ueno1, R Allen Waggoner1, Justin L Gardner1, 2, Keiji Tanaka1 & Kang Cheng1

Abstract: Although cortical neurons with similar functional properties often cluster together in a columnar organization, only ocular dominance columns, the columnar structure representing segregated anatomical input (from one of the two eyes), have been found in human primary visual cortex (V1). It has yet to be shown whether other columnar organizations that arise only from differential responses to stimulus properties also exist in human V1. Using high-resolution functional magnetic resonance imaging, we have found such a functional architecture containing domains that respond preferentially to either low or high temporal frequency.

Suggested by KGS

Specialized color modules in macaque extrastriate cortex. Conway BR, Moeller S, Tsao DY.

Imaging studies are consistent with the existence of brain regions specialized for color, but electrophysiological studies have produced conflicting results. Here we address the neural basis for color, using targeted single-unit recording in alert macaque monkeys, guided by functional magnetic resonance imaging (fMRI) of the same subjects. Distributed within posterior inferior temporal cortex, a large region encompassing V4, PITd, and posterior TEO that some have proposed functions as a single visual complex, we found color-biased fMRI hotspots that we call "globs," each several millimeters wide. Almost all cells located in globs showed strong luminance-invariant color tuning and some shape selectivity. Cells in different globs represented distinct visual field locations, consistent with the coarse retinotopy of this brain region. Cells in "interglob" regions were not color tuned, but were more strongly shape selective. Neither population was direction selective. These results suggest that color perception is mediated by specialized neurons that are clustered within the extrastriate brain.

Suggested by Bill Newsome

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