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UCSD COGS 107B - Structure and Function of Parallel Pathways

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JPhysiol 566.1 (2005) pp 13–19 13SYMPOSIUM REPORTStructure and function of parallel pathways in the primateearly visual systemEdward M. CallawaySystems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USAParallel processing streams in the primate visual system originate from more than a dozenanatomically and functionally distinct types of retinal ganglion cells (RGCs). A central problemin determining how visual information is processed is understanding how each of these RGCtypes connects to more central structures, including the lateral geniculate nucleus (LGN) of thethalamus and (via the LGN) the primary visual cortex. Neverthelss, the available functional andanatomical evidence linking together specific cell types across these structures is surprisinglyindirect. This review evaluates the available evidence and assesses the strength of the manyinferences that can be made from these observations. There is strong evidence that parasol RGCsare the provenance of the magnocellular (M) visual pathway and that midget RGCs give rise tothe parvocellular (P) pathway. Furthermore, the M and P pathways remain segregated up to theinput layer of primary visual cortex. The relationships between the numerous other RGC typesand cell types in the LGN remain less certain. and there remains ambiguity about how best todefine additional pathways, such as the koniocellular (K) pathway, which probably arise fromthese other, less common, RGC types.(Received 4 April 2005; accepted after revision 13 May 2005; first published online 19 May 2005)Corresponding author E. M. Callaway: Systems Neurobiology Laboratories, The Salk Institute for Biological Studies,10010 North Torrey Pines Road, La Jolla, CA 92037, USA. Email: [email protected] retina of the macaque monkey compacts the visualinformation received by more than 4 million cone photo-receptors and processed by millions of other retinal neuro-nes into the trains of action potentials of about 1.6 millionretinal ganglion cells (RGCs) (Rodieck, 1998). Thesesignals pass through the bottleneck of the optic nerve toconnect to a comparable number of neurones in the lateralgeniculate nucleus of the thalamus (LGN), which in turnconnect to more than 120 million neurones in the primaryvisual cortex (Van Essen et al. 1984; Beaulieu et al. 1992). Itis generally believed that the RGC signals are optimized toprovide a compact representationof the visual world,whilethe visual cortex extracts and reorganizes this informationto convert it into the signals necessary to create a coherentpercept(VanEssen et al. 1992). The strategies used tocreatecompact visual representations are apparently reflectedin the distinct properties of more than a dozen differenttypes of RGCs that project in parallel to the LGN (Daceyet al. 2003). Understanding how these parallel signalsThis report was presented at The Journal of Physiology Symposium onThe Senses, San Diego, CA, USA, 22 October 2004. It was commissionedby the Editorial Board and reflects the views of the authors.are deciphered by the visual cortex requires studies thatlink the structure and function of each pathway to thefunctional organization of visual cortex. Understandinghow parallel visual pathways are generated and comingleprovides not only information about vision, but also aframework for understanding the mechanisms by whichthe brain integrates information from multiple sources tocreate a unified, coherent percept of the external world.Acentral problem in understanding the organizationand function of parallel visual pathways is to identify thestructural and functional links between the componentneurones at successive stages in the path. Our presentevidence for such links, although in some cases strong,is surprisingly indirect. Here I focus on the evidence thatlinks together parallel neuronal subsystems from the retinathrough the primary visual cortexof the macaque monkey.Methods – their strengths and limitationsThe quality of our understanding depends onthe quality ofthe data that can be obtained to support our hypotheses.And, in turn, it also depends on the rigour with whichthe data are interpreted. Although there is ultimately noabsolute certainty, the factors which influence our levelCThe Physiological Society 2005 DOI: 10.1113/jphysiol.2005.08804714 E. M. Callaway JPhysiol 566.1of certainty are complex and also vary depending on theexperience and data available to the observer. Therefore,rather than purveying a dogmatic view of what is knownand what is left to be discovered, I prefer here to discusshypotheses in the context of the available data and themethodological strengths and limitations related to thosedata. It is therefore useful to begin by considering someof the methods that have been commonly used to linkstructure to function and to link neural systems acrossdistant structures.The most common method for identifying thefunctional properties of individual neurones isextracellular recording with metal electrodes. This methodallows unambiguous identification of the recordedneurone type only when the recording is made fromwithin a structurally and functionally uniform population.In such cases, the location of the recording can be markedby making an electrolytic lesion. This method hasbeen most useful in the LGN and V1, where relativelyhomogeneous populations can be found in distinctlayers. When such an organization exists, it is possibleto link structure and function across distant structures(e.g. retina, LGN, V1) using standard neuroanatomicaltracers. If the tracer injection is confined to particularlayers and this results in spatially localized anterograde orretrograde label, then the two functionally characterizedcompartments can be anatomically linked. It will be seen,however, that there are no locations with absolutely purepopulations that are spatially separated. Thus, there isalways some ambiguity about these links and our degreeof confidence is therefore influenced by the degree offunctional and morphological uniformity within ananatomical compartment.Unlike the LGN and V1, which have clear laminarsegregation related to the parallel pathways that emergefrom the retina, the retinal ganglion cells themselves areextensively intermingled. There is therefore little hope oflinking morphological cell types to functional propertiesbased on extracellular recordings with metal electrodes.Fortunately, in vitro retinal preparations are


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