23 Problems in Systems Neuroscience

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1 23 Problems in Systems Neuroscience Leo van Hemmen and Terrence Sejnowski (Eds) Oxford University Press, 2006 Preface J. Leo van Hemmen, Terrence J. Sejnowski 23 experts from the many areas of systems neuroscience were invited to each write a chapter that formulates one problem. Together these 23 problems provide a challenging roadmap to the field of systems neuroscience and will serve as a source of inspiration for future brain explorers. How have brains evolved? 1. "Shall we even understand the fly's brain?" Gilles Laurent I hope to illustrate two main things: the first is that small systems, and particularly small olfactory systems, seem to use mechanisms and strategies that are not unique to them. The second is that small systems are not at all that simple ; this reinforces my view that we may be better off starting with the modest goal of understanding flies first. 2. "Can we understand the action of brain in natural environments?" Hermann Wagner We work mainly on reduced systems, but evolution has shaped brains in a different way. To really understand brain function we have to analyze it in the same environment in which brains evolved. 3. Hemisphere dominance of brain function - which functions are lateralized and why? Gunther Ehret There are two main perspectives, a) an evolutionary one asking for common origins and advantages of hemisphere specializations of vertebrate, mainly mammalian, brains, and b) a proximate one asking for genetic and physiological mechanisms responsible for the realization of hemisphere specializations. How is the cerebral cortex organized? 4. What is the function of the thalamus? S. Murray Sherman The thalamus had long been thought to perform a boring, machine-like relay of information to cortex, but recent evidence suggests that it dynamically gates information flow and controls the nature of what cortex receives in a state-dependent manner. Furthermore, many areas of thalamus seem to perform a "higher-order" relay from one cortical area to another, and indeed this transthalamic route may be critical for much, perhaps all, cortico-cortical communication. 1

2 5. What is a neuronal map, how does it arise, and what is it good for? J. Leo van Hemmen Defining a `map' to be a neuronal representation of the outside world, we are facing three closely related problems: what does representation mean, how does it arise, and what is it good for? The solution to this circle of problems is fundamental to understanding how animals (and men) relate their own position to that of a stimulus in the world surrounding them. 6. What is the role of top-down connections? Jean Bullier Until recently, all models of processing of sensory information by the brain have exclusively considered a feedforward (or bottom-up) direction of information processing, with a succession of filters operating in cascade from the periphery to more "cognitive" regions of the brain. This contrasts with the presence of an enormous network of feedback connections that often outnumbers the feedforward connections and for which little is known. This essay will address a number of possible roles for these feedback connections by asking further questions : are they involved in attention?, are they involved in memory recall?, are they involved in global to local interactions? are they involved in recalibrating lower order areas following plastic changes in higher order areas? what is their role during postnatal development? It may be naive to think that a single role will be found for these top-down connections. Different sets of connections operate at different scales in terms of cortical space (some connections are focused, others are diffuse) and in terms of time (some work at the millisecond, some at the second, depending on the type of connections and receptors involved). Therefore it is likely that several of the questions asked concerning the role of top down connections will be answered in a positive manner and that one will have to think in terms of many different types of top down influences on neuronal populations. How Do Neurons Interact? 7. How fast is neuronal signal transmission? Wulfram Gerstner Starting from reaction time experiments (e.g., those of Simon Thorpe), I will argue that the standard notion that neurons or neural systems are `slow' is misleading. My specific question is: how fast can a neuronal population react to a new input? I will point out that for certain sets of parameters the response can be practically immediate. This means that integration delays are, in some cases, negligible so that only axonal delays remain. Implications for potential rapid feedback will be mentioned. 8. "What is the origin and functional properties of irregular activity?" Dr. Carl van Vreeswijk Since the work of Adrian it is known that neuronal activity varies consistently with the input/output of the cortical circuit in which the neuron is embedded. This has led to the idea of a rate code. However the activity of the neurons is very irregular, the typical coefficient of variation is about 1, so that the neuron's rate can only be inferred poorly from the number of spikes fired. It would seem 2

3 that the rate is coded inefficiently, casting doubt on the rate code assumption. In this chapter I will discuss how irregular activity could arise in highly interconnected cortical circuits, show that such a state has important functional advantages and the the disadvantages of a high CV are much smaller than commonly assumed. This suggests that the doubt about the rate code is based on a misunderstanding. 9. Are single cortical neurons independent or are they obedient members of a huge orchestra? Amiram Grinvald, Tal Kenet, Amos Arieli, Misha Tsodyks 10. What is the other 85% of V1 doing? Bruno A. Olshausen, David J. Field We pose the following challenge: that despite four decades of research characterizing the response properties of V1 neurons, we still do not have a clear picture of how V1 really operates i.e., how a population of V1 neurons represent natural scenes under realistic viewing conditions. We identify five problems with the current view that stem largely from biases in the design and execution of experiments, in addition to the contributions of non-linearities in the cortex that are not well understood. Our purpose is to open the window to new theories, a number of which we describe along with some proposals for testing them. What can brains compute? 11. What is the Formal Computation in Early Vision? Steven W. Zucker A model for early visual computations, based on a model for visual cortex in primates, will serve as an introduction to the question: "which formal computation underlies neural computation?". We will show how linear complementarity problems, quadratic programs, and polymatrix games arise. We will suggest spiking neuron methods for computing them. 12. How do neurons compute? Catherine Carr, D Soares, S Parameshwaran, S Kalluri, J Simon, T Perney An important question in neurobiology remains that of how neurons compute. Attendant on this is the question of whether neurons are designed for specific computations. We can show that some neurons are clearly designed for particular computations, presumably by natural selection. Does this mean that all neurons are designed for particular computations? Some neurons may have more general responses. Other neuron types may change their response types under the action of some modulator, but these neurons can be regarded as the case of a neuron designed for several computations, rather than for some general input-output function. To make the case that neurons in the vertebrate CNS can be designed for particular tasks, we will use the example of temporal coding cells in the auditory system because their function is well known and thus we can tie physiological and morphological observations to function. We will argue that it is important to understand the functions of single neurons. 3

4 13. "How can neural systems compute in the time domain?" Andreas V.M. Hertz Given the large variety and intriguing temporal complexity of many natural pattern sequences, sophisticated neural representations are likely to have been invented during the course of evolution. No simple, universal answer is therefore to be expected to the question posed above. Progress in the understanding of neural coding in the time domain may nevertheless be achieved if one concentrates on a more specific problem: Which types of representations best support flexible and robust computations of temporal relations? 14. How common are neural codes? David McAlpine, Alan R. Palmer The ability to localize sounds in space is a fundamental attribute of the way that humans and animals perceive their environment. It has obvious survival value in enabling them to determine where their prey or a predator is. However, unlike in vision or somato-sensation, the sensory endorgan of audition, the cochlea, contains no explicit representation of the spatial environment. Auditory space must therefore be computed indirectly from non-spatial cues. This chapter deals with the problems that the auditory system must overcome in achieving this task, and underlines the importance of understanding the specific limitations imposed by the stimulus sub-domain to which different species are responsive. Seemingly identical tasks that appear to be addressed in an identical fashion across species may require uniquely different neural codes in order to permit the extraction of useful sensory information. 15. How does the hearing system perform auditory scene analysis? Georg Klump Bregman (1990) identified a number of processes that provide for auditory object formation and auditory scene analysis. Many of these processes do not require cognitive abilities and can be found in non-human vertebrates. The chapter will review evidence for mechanisms supporting auditory object formation in animals and elucidate how these can be used for effectively analyzing natural soundscapes. 16. How does our visual system achieve shift and size invariance? Laurenz Wiskott After a short introduction about psychophysical and neurophysiological aspects of shift and size invariant recognition in the visual system an overview is given over the main computational models. Then, a few open questions and possible approaches to solving them are discussed. Shift and size invariance are just two examples of the more fundamental question of how the brain builds and learns to build invariant representations in general. 4

5 How are cognitive systems organized? 17. What is reflected in sensory neocortical activity: External stimuli or what the cortex does with them? Henning Scheich, Frank W. Ohl, Holger Schulze, Andreas Hess, Andre Brechmann Cortical activity is manifest in spatio-temporal patterns. These patterns are usually conceived as representations of stimuli in maps. Various lines of evidence suggest however that these map-based patterns also depend on the specific purpose served by the cortical processing. Therefore a broader concept of the function of sensory neocortex seems to be required. 18. "To what extent does perception depend upon action?" Giacomo Rizzolatti, Vittorio Gallese We discuss the relation between action and perception as it emerges from neurophysiological data. We propose that both action perception and space perception derive from a preceding motor knowledge based on self-generated actions. 19. "What are the projective fields of cortical neurons? Terrence J. Sejnowski The inputs to a neuron can be explored by carefully choosing the sensory stimulus, but the receptive field properties only provide part of the information needed to characterize the neuron. In addition, the impact of the neuron on other neurons needs to be assessed, called the projective field of the neuron. A broad experimental program is proposed here that could reveal the projective fields of cortical neurons, which may provide the missing information needed to unlock the mysteries of the cerebral cortex. 20. To what extent is the brain reconfigurable? John Reynolds Psychophysical and neurophysiological observations raise the question of how the different features of an object, encoded by neurons in many different areas of visual cortex, become linked together so that attending to and discriminating one feature of an object causes other features of that object to be selected, while suppressing processing of the features that make up competing objects. 21. "Where are the switches on this thing?" Laurence Abbott We know a great deal about how information relevant to sensory stimuli and motor responses is encoded in the brain. But how do we channel sensory information through the brain and activate the pathways necessary to generated appropriate responses. As well as having banks of selective representational units, the brain must involve complex switching circuitry based on biophysical mechanisms we do not yet understand. Hence the questions: where are the switches that channel information flow in the brain and how do they operate? 5

6 22 "Do qualia, metaphor, language and abstract thought emerge from synethesia?" VS Ramachandran, Edward M. Hubbard In this essay, we will consider synesthesia. First, we will show that synesthesia is a genuine sensory effect. Second, we will suggest what the underlying neural mechanisms might be. Third, we will point out that far from being just an oddity, synesthesia might help illuminate some of the most puzzling aspects of the mind such as the evolution of metaphor, language and even abstract thought in humans. In addition, we will discuss the philosophical riddle of qualia and point out how studying synesthesia and other sensory phenomena (such as the filling-in of scotomas and blind spots) can provide some hints about the evolution, functional significance and neural correlates of qualia. 23. What are the neural correlates of consciousness? Francis Crick, Christof Koch There are a host of hard problems in neuroscience, but consciousness is certainly the most mysterious of them, and so in some sense the hardest. How is one to explain qualia the redness of red or the painfulness of pain in terms of known science? So far no one has put forward any concrete hypothesis that sounds even remotely plausible. Our strategy is to leave the core of the problem on one side for the time being, and instead try first to discover the Neural Correlates of Consciousness, now widely called the NCC. 6

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