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• W2045946579 abstract "The visual cortex is not a passive recipient of information: predictions about incoming stimuli are made based on experience, partial information and the consequences of inferences. A combination of imaging studies in the human brain has now led to the proposal that the orbitofrontal cortex is a key source of top-down predictions leading to object recognition. The visual cortex is not a passive recipient of information: predictions about incoming stimuli are made based on experience, partial information and the consequences of inferences. A combination of imaging studies in the human brain has now led to the proposal that the orbitofrontal cortex is a key source of top-down predictions leading to object recognition. The study of top-down processing often reveals a paradoxical feature of how we theorise about vision. It seems that in order to explain the workings of the brain we sometimes adopt the logic of Intelligent Design — smart things can only be made by, well, by smarter things. Every visual neuroscientist has had the experience, at the end of a lecture, of being asked by an engineer in the audience “why would anyone design a system like that?” (you know it's an engineer because they always preface the question with “I am an engineer”). The answer, of course, is that nobody designed the system — it evolved. Yet when thinking about top-down control, the dominant assumption is that there must be a high-level ‘smart’ area that guides the less smart sensory cortex. This is the thinking behind the idea that the parietal or prefrontal cortices are important in top-down visual control — they are higher level areas that can somehow direct visual cortical processes [1Hung J. Driver J. Walsh V. Visual Selection and Posterior Parietal Cortex: Effects of repetitive transcranial magnetic stimulation on partial report analyzed by Bundesen's theory of visual attention.J. Neurosci. 2005; 19: 9602-9612Crossref Scopus (77) Google Scholar, 2Peers P.V. Ludwig C.J.H. Rorden C. Cusack R. Bonfiglioli C. Bundesen C. Driver J. Antoun N. Duncan J. Attentional functions of the parietal and frontal cortices.Cerebr. Cortex. 2005; 15: 1469-1484Crossref PubMed Scopus (171) Google Scholar]. The same logic guided initial theorising about cognitive contours (Figure 1). It was argued that these contours are perceived because the brain makes inferences about what kinds of objects are consistent with the retinal images with which it is presented. Such an inferential process could only be carried out by a smart area, and it was therefore assumed that the inferotemporal cortex, in some senses the pinnacle of the visual system, must be the source of the perception of cognitive contours — and neurons responding to them were duly found. Subsequent studies, however, were able to show that the architecture of visual areas V2 [3Peterhans E. von der Heydt R. Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps.J. Neurosci. 1989; 9: 1749-1763PubMed Google Scholar] and V1 [4Grosof D.H. Shapley R.M. Hawken M.J. Macaque V1 neurons can signal ‘illusory’ contours.Nature. 1993; 365: 550-552Crossref PubMed Scopus (318) Google Scholar] could be sufficient to generate these illusory percepts: could the visual cortex be smart after all? A new study [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] of visual recognition processes lends support to the idea that predictive visual processing follows a trickle-down path from frontal cortex to lower level visual areas. Previously, Bar et al. [6Bar M. Tootell R. Schacter D.L. Grieve D. Fischl B. Mendola L. Rosen B.R. Dale A.M. Cortical mechanisms of explicit visual processing.Neuron. 2001; 29: 529-535Abstract Full Text Full Text PDF PubMed Scopus (376) Google Scholar] had observed that object recognition elicited activity not only in the temporal cortex, as one might expect, but also in the orbitofrontal cortex, an area not traditionally associated with object recognition processes. In the new study, Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] presented subjects with line drawings or photographs of animals and everyday objects and subjects pressed a key if they recognised the object. Subjects underwent two types of brain imaging: functional magnetic resonance imaging (fMRI) to identify the areas activated by high or low spatial frequencies in the recognition task; and magnetoencephalography (MEG) to determine when these areas were activated. The study has three core findings: First, the MEG data showed that the right orbitofrontal cortex was activated 50 milliseconds before the right fusiform gyrus and 85 ms before the left fusiform gyrus (Figure 2). Second, activity in the orbitofrontal cortex and activity in visual areas in the temporal (fusiform gyrus) and occipital (visual cortex) lobes was time locked on a trial-by-trial basis. And third, orbitofrontal cortex activity was found to differ in response to high versus low spatial frequency stimuli (Figure 3).Figure 3High and low spatial frequency information.Show full captionImages contain different spatial frequencies. Low spatial frequencies carry ‘broad brush’ information (centre image) and high spatial frequencies carry outline and fine contour information (far right image). The initial gist of a scene may be dominated by low frequency information. From the new Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] study the proposal is that low spatial frequency information reaches the orbitofrontal cortex via fast feedforward connections and that the information is then used to generate predictions about the more detailed higher spatial frequency information coming in through the visual cortex. (Figure courtesy of Elliot Freeman.)View Large Image Figure ViewerDownload Hi-res image Download (PPT) Images contain different spatial frequencies. Low spatial frequencies carry ‘broad brush’ information (centre image) and high spatial frequencies carry outline and fine contour information (far right image). The initial gist of a scene may be dominated by low frequency information. From the new Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] study the proposal is that low spatial frequency information reaches the orbitofrontal cortex via fast feedforward connections and that the information is then used to generate predictions about the more detailed higher spatial frequency information coming in through the visual cortex. (Figure courtesy of Elliot Freeman.) On the basis of these data, Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] propose that the orbitofrontal cortex “sensitises the representation of the most likely candidate objects in the temporal cortex as a predictive initial guess”. The idea is that low spatial frequency information reaches the orbitofrontal cortex before it reaches the visual recognition areas, and that the orbitofrontal cortex sends a guiding signal to the visual recognition areas that says something like “here's a gistimate (sic) of what you're looking for”. Our engineering friend already has both hands in the air to ask the usual question, but perhaps we can also see a biologist wanting to ask a different question: why would something evolve like this? Trickle-down theories are based on movement of resources from the rich to the poor and in the case of the orbitofrontal cortex, when it comes to cognitive functions we seem to be talking about the super-rich. As Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] note, the orbitofrontal cortex is not traditionally associated with visual recognition processes, but it is associated with emotion, reward-association, impulsivity and decision making [7Cavada C. Schultz W. The mysterious orbitofrontal cortex.Cerebral Cortex. 2000; 10: 205Crossref PubMed Google Scholar, 8Kringelbach M.L. Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.Prog. Neurobiol. 2004; 71: 341-372Crossref Scopus (1483) Google Scholar]. It is also an area that receives inputs from all the senses. What we might consider, then, is whether the orbitofrontal cortex performs some function common to all its sensory inputs or whether its role in top-down visual control may be a special case. If one were to look for an explanation of the orbitofrontal cortex activations in terms of what is already known about this area, some alternative explanations begin to present themselves. The orbitofrontal cortex is indispensable for forming normal stimulus–reward associations [8Kringelbach M.L. Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.Prog. Neurobiol. 2004; 71: 341-372Crossref Scopus (1483) Google Scholar]. Hence it is possible that the orbitofrontal cortex activations seen in this study represent a prediction about the likelihood that one will identify an object correctly. In some conditions, subjects were required to indicate their level of knowledge about the object. Thus, the activations may be representative of subjects' emerging confidence in their performance on any given trial, and they could evolve in parallel and independently of visual predictive processes. Such a confidence judgement might also correlate with recognised versus unrecognised objects on a trial by trial basis. Another recent study [9Hsu M. Bhatt M. Adolphs R. Tranel D. Camerere C.F. Neural systems responding to degrees of uncertainty in human decision making.Science. 2005; 210: 1680-1683Crossref Scopus (927) Google Scholar], for example, has shown that activity in orbitofrontal cortex can correlate with a subject's level of uncertainty when making a decision. Another key question raised by the new work of Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] is whether activations in other areas that preceded orbitofrontal cortex activation could also reflect top down processing. There was greater activation for recognised versus non-recognised objects both in the early visual cortex (Figure 2) and in the right frontal eye fields (Figure 2). There is compelling evidence that the frontal eye fields play a role in top-down visual processing. The frontal eye fields respond as early as 40 milliseconds after a stimulus is presented [10Thompson K.G. Schall J.D. The detection of visual signals by macaque frontal eye field during masking.Nat. Neurosci. 1999; 2: 283-288Crossref PubMed Scopus (123) Google Scholar], have generated a representation of target location by 100–130 milliseconds [11Bichot N.P. Chenchal Rao S. Schall J.D. Continuous processing in macaque frontal cortex during visual search.Neuropsychologia. 2001; 39: 972-982Crossref PubMed Scopus (62) Google Scholar], and share topographically organised connections with a wide range of visual areas [12Schall J.D. Morel A. King D.J. Bullier J. Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams.J. Neurosci. 1995; 15: 4464-4487PubMed Google Scholar]. They are also closer than the orbitofrontal cortex to the visual areas and therefore satisfy the constraint — or at least the common observation — that evolution, like an engineer, likes to keep its wires short to limit the possibility of error [13Cowey A. Cortical maps and visual perception.Q. J. Exp. Psychol. 1979; 31: 1-17Crossref PubMed Scopus (125) Google Scholar]. There is a further reason to emphasise the role of interactions between the frontal eye field and the visual cortex. The visual areas connected to the frontal eye fields encode both low and high spatial frequency information, are closely connected to the fusiform recognition areas, and also respond to visual stimuli before the orbitofrontal cortex. It seems entirely possible that the activity in these areas preceding the orbitofrontal cortex activity (Figure 2) encapsulates all the information required for purely visual purposes prior to the fusiform activation, and that the source of the orbitofrontal cortex activity may be a parallel process representing confidence in the accuracy of the perceptual judgement that is being made under ambiguous conditions. The work of Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar] shows that even simple tasks can yield surprising and intriguing results and that understanding the temporal relationships between distant regions of cortex is a key to a more sophisticated understanding of the pathways from sense to action. The dual technique assault, adopted by Bar et al. [5Bar M. Kassa K.S. Ghuman A.S. Boshyan J. Schmidt A.M. Dale A.M. Hamalainen M.S. Marinkovic K. Schacter D.L. Rosen B.R. et al.Top-down facilitation of visual recognition.Proc. Natl. Acad. Sci. USA. 2005; 103: 449-454Crossref Scopus (1123) Google Scholar], combining fMRI and MEG, provides a richness of data that will invite new interpretations — which we hope will be a flood rather than a trickle." @default.
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• W2045946579 title "Cognitive Neuroscience: Trickle-Down Theories of Vision" @default.
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