Category selectivity in the ventral visual pathway confers robustness to clutter and diverted attention

Are objects coded by a small number of neurons or cortical regions that respond preferentially to the object in question, or by more distributed patterns of responses, including neurons or regions that respond only weakly? Distributed codes can represent a larger number of alternative items than sparse codes but produce ambiguities when multiple items are represented simultaneously (the "superposition" problem). Recent studies found category information in the distributed pattern of response across the ventral visual pathway, including in regions that do not "prefer" the object in question. However, these studies measured neural responses to isolated objects, a situation atypical of real-world vision, where multiple objects are usually present simultaneously ("clutter"). We report that information in the spatial pattern of fMRI response about standard object categories is severely disrupted by clutter and eliminated when attention is diverted. However, information about preferred categories in category-specific regions is undiminished by clutter and partly preserved under diverted attention. These findings indicate that in natural conditions, the pattern of fMRI response provides robust category information only for objects coded in selective cortical regions and highlight the vulnerability of distributed representations to clutter and the advantages of sparse cortical codes in mitigating clutter costs.     

Visual saliency and spike timing in the ventral visual pathway.

Visual saliency is a fundamental yet hard to define property of objects or locations in the visual world. In a context where objects and their representations compete to dominate our perception, saliency can be thought of as the "juice" that makes objects win the race. It is often assumed that saliency is extracted and represented in an explicit saliency map, which serves to determine the location of spatial attention at any given time. It is then by drawing attention to a salient object that it can be recognized or categorized. I argue against this classical view that visual "bottom-up" saliency automatically recruits the attentional system prior to object recognition. A number of visual processing tasks are clearly performed too fast for such a costly strategy to be employed. Rather, visual attention could simply act by biasing a saliency-based object recognition system. Under natural conditions of stimulation, saliency can be represented implicitly throughout the ventral visual pathway, independent of any explicit saliency map. At any given level, the most activated cells of the neural population simply represent the most salient locations. The notion of saliency itself grows increasingly complex throughout the system, mostly based on luminance contrast until information reaches visual cortex, gradually incorporating information about features such as orientation or color in primary visual cortex and early extrastriate areas, and finally the identity and behavioral relevance of objects in temporal cortex and beyond. Under these conditions the object that dominates perception, i.e. the object yielding the strongest (or the first) selective neural response, is by definition the one whose features are most "salient"--without the need for any external saliency map. In addition, I suggest that such an implicit representation of saliency can be best encoded in the relative times of the first spikes fired in a given neuronal population. In accordance with our subjective experience that saliency and attention do not modify the appearance of objects, the feed-forward propagation of this first spike wave could serve to trigger saliency-based object recognition outside the realm of awareness, while conscious perceptions could be mediated by the remaining discharges of longer neuronal spike trains.     

Fast and automatic activation of an abstract representation of money in the human ventral visual pathway

Money, when used as an incentive, activates the same neural circuits as rewards associated with physiological needs. However, unlike physiological rewards, monetary stimuli are cultural artifacts: how are monetary stimuli identified in the first place? How and when does the brain identify a valid coin, i.e. a disc of metal that is, by social agreement, endowed with monetary properties? We took advantage of the changes in the Euro area in 2002 to compare neural responses to valid coins (Euros, Australian Dollars) with neural responses to invalid coins that have lost all monetary properties (French Francs, Finnish Marks). We show in magneto-encephalographic recordings, that the ventral visual pathway automatically distinguishes between valid and invalid coins, within only ∼150 ms. This automatic categorization operates as well on coins subjects were familiar with as on unfamiliar coins. No difference between neural responses to scrambled controls could be detected. These results could suggest the existence of a generic, all-purpose neural representation of money that is independent of experience. This finding is reminiscent of a central assumption in economics, money fungibility, or the fact that a unit of money is substitutable to another. From a neural point of view, our findings may indicate that the ventral visual pathway, a system previously thought to analyze visual features such as shape or color and to be influenced by daily experience, could also able to use conceptual attributes such as monetary validity to categorize familiar as well as unfamiliar visual objects. The symbolic abilities of the posterior fusiform region suggested here could constitute an efficient neural substrate to deal with culturally defined symbols, independently of experience, which probably fostered money''s cultural emergence and success.     

Transformation of shape information in the ventral pathway

Object perception seems effortless to us, but it depends on intensive neural processing across multiple stages in ventral pathway visual cortex. Shape information at the retinal level is hopelessly complex, variable and implicit. The ventral pathway must somehow transform retinal signals into much more compact, stable and explicit representations of object shape. Recent findings highlight key aspects of this transformation: higher-order contour derivatives, structural representation in object-based coordinates, composite shape tuning dimensions, and long-term storage of object knowledge. These coding principles could help to explain our remarkable ability to perceive, distinguish, remember and understand a virtual infinity of objects.     

Allocentric representation in the human amygdala and ventral visual stream

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Invariance of visual operations at the level of receptive fields

The brain is able to maintain a stable perception although the visual stimuli vary substantially on the retina due to geometric transformations and lighting variations in the environment. This paper presents a theory for achieving basic invariance properties already at the level of receptive fields. Specifically, the presented framework comprises (i) local scaling transformations caused by objects of different size and at different distances to the observer, (ii) locally linearized image deformations caused by variations in the viewing direction in relation to the object, (iii) locally linearized relative motions between the object and the observer and (iv) local multiplicative intensity transformations caused by illumination variations. The receptive field model can be derived by necessity from symmetry properties of the environment and leads to predictions about receptive field profiles in good agreement with receptive field profiles measured by cell recordings in mammalian vision. Indeed, the receptive field profiles in the retina, LGN and V1 are close to ideal to what is motivated by the idealized requirements. By complementing receptive field measurements with selection mechanisms over the parameters in the receptive field families, it is shown how true invariance of receptive field responses can be obtained under scaling transformations, affine transformations and Galilean transformations. Thereby, the framework provides a mathematically well-founded and biologically plausible model for how basic invariance properties can be achieved already at the level of receptive fields and support invariant recognition of objects and events under variations in viewpoint, retinal size, object motion and illumination. The theory can explain the different shapes of receptive field profiles found in biological vision, which are tuned to different sizes and orientations in the image domain as well as to different image velocities in space-time, from a requirement that the visual system should be invariant to the natural types of image transformations that occur in its environment.     

fMRI reveals how pain modulates visual object processing in the ventral visual stream

It is well known that pain attracts attention and interferes with cognition. Given that the mechanisms behind this phenomenon are largely unknown, we used functional magnetic resonance imaging and presented visual objects with or without concomitant pain stimuli. To test for the specificity of pain, we compared this modulatory effect with a previously established modulatory effect of working memory on visual object processing. Our data showed a comparable behavioral effect of both types of modulation and identified the lateral occipital complex (LOC) as the site of modulation in the ventral visual stream, for both pain and working memory. However, the sources of these modulatory effects differed for the two processes. Whereas the source of modulation for working memory could be attributed to the parietal cortex, the modulatory effect of pain was observed in the rostral anterior cingulate cortex (rACC), an area ideally suited to link pain perception and attentional control.     

Orientation selectivity and visual acuity in schoolchildren and adults

We continued our study of the mechanisms of visual acuity (VA) in ontogenesis. We measured the VA and sensitivity to lines orientation and determined the minimal length of lines for discrimination of the vertical and the horizontal ones in subjects aged 7–25 years. It was found that the thresholds of discrimination of vertical and horizontal lines in subjects with normal VA decreased with age up to 9–10 years and then remained constant, while the orientation selectivity was improving up to the age of 14–16 years. The average VA almost did not depend on age. Individual thresholds of line lengths and orientation discrimination correlated with the VA of subjects.     

Similarity of visual selectivity among clonally related neurons in visual cortex

Neurons in rodent visual cortex are organized in a salt-and-pepper fashion for orientation selectivity, but it is still unknown how this functional architecture develops. A recent study reported that the progeny of single cortical progenitor cells are preferentially connected in the postnatal cortex. If these neurons acquire similar selectivity through their connections, a salt-and-pepper organization may be generated, because neurons derived from different progenitors are intermingled in rodents. Here we investigated whether clonally related cells have similar preferred orientation by using a transgenic mouse, which labels all the progeny of single cortical progenitor cells. We found that preferred orientations of clonally related cells are similar to each other, suggesting that cell lineage is involved in the development of response selectivity of neurons in the cortex. However, not all clonally related cells share response selectivity, suggesting that cell lineage is not the only determinant of response selectivity.     

A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord.

Sonic hedgehog (Shh) is thought to control the generation of motor neurons and interneurons in the ventral CNS. We show here that a Shh-independent pathway of interneuron generation also operates in the ventral spinal cord. Evidence for this parallel pathway emerged from an analysis of the induction of ventral progenitors that express the Dbx homeodomain proteins and of Evx1/2 (V0) and En1 (V1) neurons. Shh signaling is sufficient to induce Dbx cells and V0 and V1 neurons but is not required for their generation in vitro or in vivo. Retinoids appear to mediate this parallel pathway. These findings reveal an unanticipated Shh-independent signaling pathway that controls progenitor cell identity and interneuron diversity in the ventral spinal cord.     

Cysteine sulfinate carboxylase in the visual pathway of adult chicken.

Cysteine sulfinate (CSA) carboxylyase, the enzyme which synthesizes taurine through hypotaurine, shows a higher activity in the inner plexiform and nuclear layer of adult chick retina compared to the outer plexiform and nuclear layers whereas the outer segments of photoreceptors do not show any activity of this enzyme. These observations suggest an endogenous synthesis of taurine preferentially in certain layers of retina. Therefore, taurine fulfills one more criteria which is required by a substance to be accepted as a neurotransmitter in an organ. Studies on the distribution of CSA-carboxylyase in the visual pathway and other brain areas show a very high activity of this enzyme in optic tectum followed by cerebral cortex, cerebellum, retina, lateral geniculate body and optic nerve, taken with chiasma and tract in decreasing order. On the other hand, analysis of the free amino acid pool reveals a very high content of taurine in retina as compared to optic tectum. Cysteine sulfinate carboxylyase activity and the content of taurine therefore do not seem to bear a good correlation and other mechanisms of release, uptake and degradation might be involved in regulating the taurine content in these tissues.     

Spike timing and visual processing in the retinogeniculocortical pathway

Although the visual response properties of neurons along the retinogeniculocortical pathway have been studied for decades, relatively few studies have examined how individual neurons along the pathway communicate with each other. Recent studies in the cat (Felis domestica) now show that the strength of these connections is very dynamic and spike timing plays an important part in determining whether action potentials will be transferred from pre- to postsynaptic cells. This review explores recent progress in our understanding of what role spike timing has in establishing different patterns of geniculate activity and how these patterns ultimately drive the cortex.     

Effective connectivity of dorsal and ventral visual pathways in chunk decomposition

Chunk decomposition is defined as a cognitive process which breaks up familiar items into several parts to reorganize them in an alternative approach. The present study investigated the effective connectivity of visual streams in chunk decomposition through dynamic causal modeling (DCM). The results revealed that chunk familiarity and perceptual tightness made a combined contribution to highlight not only the “what” and the “where” streams, but also the effective connectivity from the left inferior temporal gyrus to the left superior parietal lobule.     

Profound contrast adaptation early in the visual pathway

Prior exposure to a moving grating of high contrast led to a substantial and persistent reduction in the contrast sensitivity of neurons in the lateral geniculate nucleus (LGN) of macaque. This slow contrast adaptation was potent in all magnocellular (M) cells but essentially absent in parvocellular (P) cells and neurons that received input from S cones. Simultaneous recordings of M cells and the potentials of ganglion cells driving them showed that adaptation originated in ganglion cells. As expected from the spatiotemporal tuning of M cells, adaptation was broadly tuned for spatial frequency and lacked orientation selectivity. Adaptation could be induced by high temporal frequencies to which cortical neurons do not respond, but not by low temporal frequencies that can strongly adapt cortical neurons. Our observations confirm that contrast adaptation occurs at multiple levels in the visual system, and they provide a new way to reveal the function and perceptual significance of the M pathway.     

Goal-related activity in V4 during free viewing visual search. Evidence for a ventral stream visual salience map

Natural exploration of complex visual scenes depends on saccadic eye movements toward important locations. Saccade targeting is thought to be mediated by a retinotopic map that represents the locations of salient features. In this report, we demonstrate that extrastriate ventral area V4 contains a retinotopic salience map that guides exploratory eye movements during a naturalistic free viewing visual search task. In more than half of recorded cells, visually driven activity is enhanced prior to saccades that move the fovea toward the location previously occupied by a neuron's spatial receptive field. This correlation suggests that bottom-up processing in V4 influences the oculomotor planning process. Half of the neurons also exhibit top-down modulation of visual responses that depends on search target identity but not visual stimulation. Convergence of bottom-up and top-down processing streams in area V4 results in an adaptive, dynamic map of salience that guides oculomotor planning during natural vision.     

Cognitive set depends on the involvement of the ventral and dorsal visual systems

Healthy adults were examined in three series of experiments with formation of an unconscious visual set: 1) the set was formed by repeated presentation of pairs of unequal circles (control); 2) an additional task of recognition of words/pseudowords was introduced into the context of the set-forming trials; 3) in the task additionally introduced, a subject had to spatially localize a certain target letter in a letter matrix. Scores of stability of the visual set to circles were compared. Coherence of the cortical electric activity in the alpha band was analyzed. We revealed a significant decrease in stability (rigidity) of the nonverbal visual set in the series with the additional task of spatial localization of the target stimulus. On the contrary, the set rigidity increased in the series with additional recognition of the verbal stimulus. EEG coherence patterns and behavioral data suggest that successful cognitive performance that demands dynamic situation-dependent shifts of unconscious sets takes place under conditions of alternation of tasks involving, predominantly, either the ventral ("what?") or dorsal ("where?") visual streams and, respectively, anterior or posterior systems of selective attention.