Object Category Structure in Response Patterns of Neuronal Population in Monkey Inferior Temporal Cortex

Roozbeh Kiani, Hossein Esteky, Koorosh Mirpour, Keiji Tanaka
J Neurophysiol (April 11, 2007). doi:10.1152/jn.00024.2007

Our mental representation of object categories is hierarchically organized, and our rapid and seemingly effortless categorization ability is crucial for our daily behavior. Here, we examine responses of a large number (>600) of neurons in monkey inferior temporal (IT) cortex with a large number (>1000) of natural and artificial object images. During the recordings the monkeys performed a passive fixation task. We found that the categorical structure of objects is represented by the pattern of activity distributed over the cell population. Animate and inanimate objects created distinguishable clusters in the population code. The global category of animate objects was divided into bodies, hands and faces. Faces were divided into primate and non-primate faces, and the primate-face group was divided into human and monkey faces. Bodies of human, birds, and four-limb animals clustered together, while lower animals such as fish, reptile and insects made another cluster. Thus, the cluster analysis showed that IT population responses reconstruct a large part of our intuitive category structure, including the global division into animate and inanimate objects, and further hierarchical subdivisions of animate objects. The representation of categories was distributed in several respects, e.g., the similarity of response patterns to stimuli within a category was maintained by both the cells that maximally responded to the category and the cells that responded weakly to the category. These results advance our understanding of the nature of the IT neural code, suggesting an inherently categorical representation that comprises a range of categories including the amply investigated face category.

Fulltext: http://jn.physiology.org/cgi/reprint/00024.2007v1

Context-dependent perceptual modulation of single neurons in primate visual cortex

Alexander Maier, Nikos K. Logothetis, David A. Leopold
Proc Natl Acad Sci U S A. 2007 March 27; 104(13): 5620–5625.

Some neurons in the visual cortex alter their spiking rate according to the perceptual interpretation of an observed stimulus, rather than its physical structure alone. Experiments in monkeys have suggested that, although the proportion of neurons showing this effect differs greatly between cortical areas, this proportion remains similar across different stimuli. These findings have raised the intriguing questions of whether the same neurons always participate in the disambiguation of sensory patterns and whether such neurons might represent a special class of cortical cells that relay perceptual signals to higher cortical areas. Here we explore this question by measuring activity in the middle temporal cortex of monkeys and asking to what degree the percept-related responses of individual neurons depend upon the specific sensory input. In contrast to our expectations, we found that even small differences in the stimuli led to significant changes in the signaling of the perceptual state by single neurons. We conclude that nearly all feature-responsive neurons in this area, rather than a select subset, can contribute to the resolution of sensory conflict, and that the role of individual cells in signaling the perceptual outcome is tightly linked to the fine details of the stimuli involved.

Free Fulltext: http://www.pnas.org/cgi/reprint/104/13/5620

Attentional Load Modulates Responses of Human Primary Visual Cortex to Invisible Stimuli

Bahador Bahrami, Nilli Lavie, Geraint Rees
Current Biology, 2007, 17:6:R202-R203

Visual neuroscience has long sought to determine the extent to which stimulus-evoked activity in visual cortex depends on attention and awareness. Some influential theories of consciousness maintain that the allocation of attention is restricted to conscious representations. However, in the load theory of attention, competition between task-relevant and task-irrelevant stimuli for limited-capacity attention does not depend on conscious perception of the irrelevant stimuli. The critical test is whether the level of attentional load in a relevant task would determine unconscious neural processing of invisible stimuli. Human participants were scanned with high-field fMRI while they performed a foveal task of low or high attentional load. Irrelevant, invisible monocular stimuli were simultaneously presented peripherally and were continuously suppressed by a flashing mask in the other eye. Attentional load in the foveal task strongly modulated retinotopic activity evoked in primary visual cortex (V1) by the invisible stimuli. Contrary to traditional views, we found that availability of attentional capacity determines neural representations related to unconscious processing of continuously suppressed stimuli in human primary visual cortex. Spillover of attention to cortical representations of invisible stimuli (under low load) cannot be a sufficient condition for their awareness.

Fulltext: http://download.current-biology.com/pdfs/0960-9822/PIIS0960982207008779.pdf

A new perceptual illusion reveals mechanisms of sensory decoding

Jazayeri M, Movshon JA.
Nature. 2007 Apr 4

Perceptual illusions are usually thought to arise from the way sensory signals are encoded by the brain, and indeed are often used to infer the mechanisms of sensory encoding. But perceptual illusions might also result from the way the brain decodes sensory information, reflecting the strategies that optimize performance in particular tasks. In a fine discrimination task, the most accurate information comes from neurons tuned away from the discrimination boundary, and observers seem to use signals from these 'displaced' neurons to optimize their performance. We wondered whether using signals from these neurons might also bias perception. In a fine direction discrimination task using moving random-dot stimuli, we found that observers' perception of the direction of motion is indeed biased away from the boundary. This misperception can be accurately described by a decoding model that preferentially weights signals from neurons whose responses best discriminate those directions. In a coarse discrimination task, to which a different decoding rule applies, the same stimulus is not misperceived, suggesting that the illusion is a direct consequence of the decoding strategy that observers use to make fine perceptual judgments. The subjective experience of motion is therefore not mediated directly by the responses of sensory neurons, but is only developed after the responses of these neurons are decoded.

PMID: 17410125

Fulltext: http://www.nature.com/nature/journal/vaop/ncurrent/pdf/nature05739.pdf

Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex

Franco L, Rolls ET, Aggelopoulos NC, Jerez JM
Biol Cybern. 2007 Apr 5

The sparseness of the encoding of stimuli by single neurons and by populations of neurons is fundamental to understanding the efficiency and capacity of representations in the brain, and was addressed as follows. The selectivity and sparseness of firing to visual stimuli of single neurons in the primate inferior temporal visual cortex were measured to a set of 20 visual stimuli including objects and faces in macaques performing a visual fixation task. Neurons were analysed with significantly different responses to the stimuli. The firing rate distribution of 36% of the neurons was exponential. Twenty-nine percent of the neurons had too few low rates to be fitted by an exponential distribution, and were fitted by a gamma distribution. Interestingly, the raw firing rate distribution taken across all neurons fitted an exponential distribution very closely. The sparseness a (s) or selectivity of the representation of the set of 20 stimuli provided by each of these neurons (which takes a maximal value of 1.0) had an average across all neurons of 0.77, indicating a rather distributed representation. The sparseness of the representation of a given stimulus by the whole population of neurons, the population sparseness a (p), also had an average value of 0.77. The similarity of the average single neuron selectivity a (s) and population sparseness for any one stimulus taken at any one time a (p) shows that the representation is weakly ergodic. For this to occur, the different neurons must have uncorrelated tuning profiles to the set of stimuli.

PMID: 17410377
Fulltext: http://www.springerlink.com/content/a4p65q184v634463/fulltext.pdf

A New Code for Contrast in the Primate Visual Pathway

Chris Tailby, Samuel G. Solomon, Neel T. Dhruv, Najib J. Majaj, Sach H. Sokol, Peter Lennie
The Journal of Neuroscience, April 4, 2007, 27(14):3904-3909;

We characterize a hitherto undocumented type of neuron present in the regions bordering the principal layers of the macaque lateral geniculate nucleus. Neurons of this type were distinguished by a high and unusually regular maintained discharge that was suppressed by spatiotemporal modulation of luminance or chromaticity within the receptive field. The response to any effective stimulus was a reduction in discharge, reminiscent of the "suppressed-by-contrast" cells of the cat retina. To a counterphase-modulated grating, the response was a phase-insensitive suppression modulated at twice the stimulus frequency, implying a receptive field comprised of multiple mechanisms that generate rectifying responses. This distinctive nonlinearity makes the neurons well suited to computing a measure of contrast energy; such a signal might be important in regulating sensitivity early in visual cortex.

Fulltext: http://www.jneurosci.org/cgi/reprint/27/14/3904

The Cortical Representation of Objects Rotating in Depth

Sarah Weigelt, Zoe Kourtzi, Axel Kohler, Wolf Singer, Lars Muckli
The Journal of Neuroscience, April 4, 2007, 27(14):3864-3874;

The perception of motion provides valuable interpolations of the visual scene. This fundamental capacity of the visual system is evident in apparent rotation: by presenting only two images of an object rotated in space, a vivid illusion of a smooth apparent motion in three dimensions can be induced. The unseen interpolated rotation views are filled in by the visual system. In the present study, we identified the cortical network responsible for this filling-in process. We argue that cross talk between areas of the ventral and dorsal visual pathways promote the illusion of smooth apparent rotation. Most interestingly, the network represents the unseen object views. Using functional magnetic resonance adaptation, we are able to show that the cortical network selectively adapts to the illusory object views. Our findings provide strong evidence for cortical representations of three-dimensional rotating objects that are view invariant with respect to the rotation path. Furthermore, our results confirm psychophysical investigations that unseen interpolated rotation views can be primed by apparent motion. By applying functional magnetic resonance adaptation, we show for the first time cortical adaptation to unseen objects. Together, our neuroimaging study advances the understanding of the cortical mechanisms mediating the influence of motion on object processing.

Neural encoding of the concept of nest in the mouse brain

Longnian Lin, Guifen Chen, Hui Kuang, Dong Wang, and Joe Z. Tsien
PNAS | April 3, 2007 | vol. 104 | no. 14 | 6066-6071

As important as memory is to our daily functions, the ability to extract fundamental features and commonalities from various episodic experiences and to then generalize them into abstract concepts is even more crucial for both humans and animals to adapt to novel and complex situations. Here, we report the neural correlates of the abstract concept of nests or beds in mice. Specifically, we find hippocampal neurons that selectively fire or cease to fire when the mouse perceives nests or beds, regardless of their locations and environments. Parametric analyses show that responses of nest cells remain invariant over changes in the nests' physical shape, style, color, odor, or construction materials; rather, their responses are driven by conscious awareness and physical determination of the categorical features that would functionally define nests. Such functionality-based abstraction and generalization of conceptual knowledge, emerging from episodic experiences, suggests that the hippocampus is an intrinsic part of the hierarchical structure for generating concepts and knowledge in the brain.

Free Fulltext: http://www.pnas.org/cgi/reprint/104/14/6066

Multiple-Color Optical Activation, Silencing, and Desynchronization of Neural Activity, with Single-Spike Temporal Resolution

Xue Han, Edward S. Boyden
PLoS ONE 2(3): e299. doi:10.1371/journal.pone.0000299

The quest to determine how precise neural activity patterns mediate computation, behavior, and pathology would be greatly aided by a set of tools for reliably activating and inactivating genetically targeted neurons, in a temporally precise and rapidly reversible fashion. Having earlier adapted a light-activated cation channel, channelrhodopsin-2 (ChR2), for allowing neurons to be stimulated by blue light, we searched for a complementary tool that would enable optical neuronal inhibition, driven by light of a second color. Here we report that targeting the codon-optimized form of the light-driven chloride pump halorhodopsin from the archaebacterium Natronomas pharaonis (hereafter abbreviated Halo) to genetically-specified neurons enables them to be silenced reliably, and reversibly, by millisecond-timescale pulses of yellow light. We show that trains of yellow and blue light pulses can drive high-fidelity sequences of hyperpolarizations and depolarizations in neurons simultaneously expressing yellow light-driven Halo and blue light-driven ChR2, allowing for the first time manipulations of neural synchrony without perturbation of other parameters such as spiking rates. The Halo/ChR2 system thus constitutes a powerful toolbox for multichannel photoinhibition and photostimulation of virally or transgenically targeted neural circuits without need for exogenous chemicals, enabling systematic analysis and engineering of the brain, and quantitative bioengineering of excitable cells.

Free Fulltext: http://www.plosone.org/article/fetchArticle.action?articleURI=info:doi/10.1371/journal.pone.0000299

First-spike latency information in single neurons increases when referenced to population onset

Steven M. Chase, and  Eric D. Young
PNAS | March 20, 2007 | vol. 104 | no. 12 | 5175-5180

It is well known that many stimulus parameters, such as sound location in the auditory system or contrast in the visual system, can modulate the timing of the first spike in sensory neurons. Could first-spike latency be a candidate neural code? Most studies measuring first-spike latency information assume that the brain has an independent reference for stimulus onset from which to extract latency. This assumption creates an obvious confound that casts doubt on the feasibility of first-spike latency codes. If latency is measured relative to an internal reference of stimulus onset calculated from the responses of the neural population, the information conveyed by the latency of single neurons might decrease because of correlated changes in latency across the population. Here we assess the effects of a realistic model of stimulus onset detection on the first-spike latency information conveyed by single neurons in the auditory system. Contrary to expectation, we find that on average, the information contained in single neurons does not decrease; in fact, the majority of neurons show a slight increase in the information conveyed by latency referenced to a population onset. Our results show that first-spike latency codes are a feasible mechanism for information transfer even when biologically plausible estimates of stimulus onset are taken into account.

Free Fulltext: http://www.pnas.org/cgi/reprint/104/12/5175


Keywords: coding, inferior colliculus, mutual information, sound localization

Differential development of high-level visual cortex correlates with category-specific recognition memory

Golijeh Golarai, Dara G Ghahremani, S Whitfield-Gabrieli, Allan Reiss, Jennifer L Eberhardt, John D E Gabrieli, Kalanit Grill-Spector
Nature Neuroscience   - 10, 512 - 522 (2007)

High-level visual cortex in humans includes functionally defined regions that preferentially respond to objects, faces and places. It is unknown how these regions develop and whether their development relates to recognition memory. We used functional magnetic resonance imaging to examine the development of several functionally defined regions including object (lateral occipital complex, LOC)-, face ('fusiform face area', FFA; superior temporal sulcus, STS)- and place ('parahippocampal place area', PPA)-selective cortices in children (ages 7–11), adolescents (12–16) and adults. Right FFA and left PPA volumes were substantially larger in adults than in children. This development occurred by expansion of FFA and PPA into surrounding cortex and was correlated with improved recognition memory for faces and places, respectively. In contrast, LOC and STS volumes and object-recognition memory remained constant across ages. Thus, the ventral stream undergoes a prolonged maturation that varies temporally across functional regions, is determined by brain region rather than stimulus category, and is correlated with the development of category-specific recognition memory.


Fulltext: http://www.nature.com/neuro/journal/v10/n4/pdf/nn1865.pdf

Neural mechanisms for timing visual events are spatially selective in real-world coordinates

David Burr, Arianna Tozzi, M Concetta Morrone
Nature Neuroscience   - 10, 423 - 425 (2007)  

It is generally assumed that perceptual events are timed by a centralized supramodal clock. This study challenges this notion in humans by providing clear evidence that visual events of subsecond duration are timed by visual neural mechanisms with spatially circumscribed receptive fields, localized in real-world, rather than retinal, coordinates.

Fulltext: http://www.nature.com/neuro/journal/v10/n4/pdf/nn1874.pdf

Controlling for interstimulus perceptual variance abolishes N170 face selectivity

Guillaume Thierry, Clara D Martin, Paul Downing, Alan J Pegna
Nature Neuroscience   - 10, 505 - 511 (2007)  

Establishing when and how the human brain differentiates between object categories is key to understanding visual cognition. Event-related potential (ERP) investigations have led to the consensus that faces selectively elicit a negative wave peaking 170 ms after presentation, the 'N170'. In such experiments, however, faces are nearly always presented from a full front view, whereas other stimuli are more perceptually variable, leading to uncontrolled interstimulus perceptual variance (ISPV). Here, we compared ERPs elicited by faces, cars and butterflies while—for the first time—controlling ISPV (low or high). Surprisingly, the N170 was sensitive, not to object category, but to ISPV. In addition, we found category effects independent of ISPV 70 ms earlier than has been generally reported. These results demonstrate early ERP category effects in the visual domain, call into question the face selectivity of the N170 and establish ISPV as a critical factor to control in experiments relying on multitrial averaging.

Fulltext: http://www.nature.com/neuro/journal/v10/n4/pdf/nn1864.pdf

Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain

Hans-Ulrich Dodt, Ulrich Leischner, Anja Schierloh, Nina Jährling, Christoph Peter Mauch, Katrin Deininger, Jan Michael Deussing, Matthias Eder, Walter Zieglgänsberger & Klaus Becker
Nature Methods   - 4, 331 - 336 (2007)  



Free Videos from Nature.com:

Supplementary Video 1 ( mov 3M)
whole mouse brain reconstructed from 550 optical sections.

Supplementary Video 2 ( mov 3M)
Granule cells with dendrites in the hippocampus of a thy-1 GFP mouse.

Supplementary Video 3 (mov 1020K)
Excised whole hippocampus.

Supplementary Video 4 ( mov 1M)
Optical sectioning of a whole hippocampus.

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3D-reconstruction and animation of a part of a whole hippocampus.

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3D reconstruction and animation of axonal bundles in the hippocampal alveus and dendritic spines of CA1 pyramidal neurons.

Supplementary Video 7 (mov 1M)
Primary and secondary barrel field made visible by excitation of autofluorescence in the whole brain of a 10 day old mouse.

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Optical sectioning of a mouse brain imaged by detection of scattered light. Note the appearance of fibre tracts during the movement of the optical sectioning plane through the brain.

Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices

Buschman TJ, Miller EK
Science. 2007 Mar 30;315(5820):1860-2

Attention can be focused volitionally by "top-down" signals derived from task demands and automatically by "bottom-up" signals from salient stimuli. The frontal and parietal cortices are involved, but their neural activity has not been directly compared. Therefore, we recorded from them simultaneously in monkeys. Prefrontal neurons reflected the target location first during top-down attention, whereas parietal neurons signaled it earlier during bottom-up attention. Synchrony between frontal and parietal areas was stronger in lower frequencies during top-down attention and in higher frequencies during bottom-up attention. This result indicates that top-down and bottom-up signals arise from the frontal and sensory cortex, respectively, and different modes of attention may emphasize synchrony at different frequencies.

PMID: 17395832

The proprioceptive representation of eye position in monkey primary somatosensory cortex

Wang X, Zhang M, Cohen IS, Goldberg ME
Nat Neurosci. 2007 Apr 1;

The cerebral cortex must have access to an eye position signal, as humans can report passive changes in eye position in total darkness, and visual responses in many cortical areas are modulated by eye position. The source of this signal is unknown. Here we demonstrate a representation of eye position in monkey primary somatosensory cortex, in the representation of the trigeminal nerve, near cells with a tactile representation of the contralateral brow. The neurons have eye position signals that increase monotonically with increasing orbital eccentricity from near the center of gaze, with directionally selectivity tuned in a Gaussian manner. All directions of eye position are represented in a single hemisphere. The signal is proprioceptive, because it can be obliterated by anesthetizing the contralateral orbit. It is not related to foveal or peripheral visual stimulation, and it represents the position of the eye in the head and not the angle of gaze in space.

PMID: 17396123
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