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Information Processing in the Primate Retina: Circuitry and Coding ANRV314-NE30-01 ARI 7 May 2007 17:2 Information Processing in the Primate Retina: Circuitry and Coding G.D. Field and E.J. Chichilnisky The Salk Institute, La Jolla, California 92037; email: [email protected] Annu. Rev. Neurosci. 2007. 30:1–30 Key Words First published online as a Review in Advance on vision, parallel pathways, neural coding, synchrony, retinal March 2, 2007 ganglion cells The Annual Review of Neuroscience is online at by 69.200.94.6 on 07/11/07. For personal use only. neuro.annualreviews.org Abstract This article’s doi: The function of any neural circuit is governed by connectivity of 10.1146/annurev.neuro.30.051606.094252 neurons in the circuit and the computations performed by the neu- Copyright c 2007 by Annual Reviews. rons. Recent research on retinal function has substantially advanced All rights reserved Annu. Rev. Neurosci. 2007.30:1-30. Downloaded from arjournals.annualreviews.org understanding in both areas. First, visual information is transmitted 0147-006X/07/0721-0001$20.00 to the brain by at least 17 distinct retinal ganglion cell types de- fined by characteristic morphology, light response properties, and central projections. These findings provide a much more accurate view of the parallel visual pathways emanating from the retina than do previous models, and they highlight the importance of identify- ing distinct cell types and their connectivity in other neural circuits. Second, encoding of visual information involves significant tempo- ral structure and interactions in the spike trains of retinal neurons. The functional importance of this structure is revealed by computa- tional analysis of encoding and decoding, an approach that may be applicable to understanding the function of other neural circuits. 1 ANRV314-NE30-01 ARI 7 May 2007 17:2 In the first section, Many Distinct Path- Contents ways of Visual Information Emanate from the Retina, we argue that the textbook view of INTRODUCTION................. 2 three primary parallel pathways carrying vi- Overview ........................ 2 sual information from retina to thalamus and Scope ............................ 3 cortex is grossly oversimplified. The subdi- MANY DISTINCT PATHWAYS OF vision of retinal output signals into parallel VISUAL INFORMATION pathways with distinct physiological proper- EMANATE FROM THE ties and central projections has been appre- RETINA ........................ 3 ciated for decades, and its functional impor- Background ...................... 3 tance has been explored in numerous studies. Advances......................... 3 However, recent findings have dramatically Implications...................... 11 expanded and clarified our understanding of PRECISION OF RETINAL SPIKE these parallel pathways. This expansion and TRAINS AND MODELS OF clarification have major implications for un- THE NEURAL CODE .......... 12 derstanding the function of the visual system Background ...................... 12 and highlight the need for focused effort to Advances......................... 12 identify the distinct functions and central pro- Implications...................... 15 jections of each retinal pathway. SYNCHRONIZED FIRING AND In the subsequent three sections, Preci- CONSEQUENCES FOR sion of Retinal Spike Trains and Models of VISUAL SIGNALING .......... 15 the Neural Code, Synchronized Firing and Background ...................... 15 Consequences for Visual Signaling, and De- Advances......................... 15 coding the Visual Signal from Retinal Spike Implications...................... 18 Trains, we discuss transmission of visual in- DECODING THE VISUAL formation from the retina to the brain and SIGNAL FROM RETINAL the consequent impact on decoding by down- SPIKE TRAINS ................. 18 stream structures. In recent years, empiri- Background ...................... 18 cal findings have revealed that retinal spike Advances......................... 19 trains are significantly more complex than Implications...................... 20 was commonly appreciated, exhibiting sur- by 69.200.94.6 on 07/11/07. For personal use only. CONCLUSIONS................... 21 prisingly precise spike timing and highly structured concerted activity in different cells. Modeling efforts have been aimed at captur- INTRODUCTION ing the complexity of retinal ganglion cell Annu. Rev. Neurosci. 2007.30:1-30. Downloaded from arjournals.annualreviews.org (RGC) spike trains evoked by visual stimuli Overview and revealing the resulting constraints on de- A central goal of neuroscience is to under- coding in central visual structures. Progress stand how information is processed in neural in these areas has significant implications for circuits. This goal poses at least two major understanding the function of other neural challenges. First, one must identify the dis- circuits. tinct cell types and connectivity in the circuit. In the concluding section, we provide a Second, one must describe the computations brief summary of how the progress described performed by the neurons and how the results above clarifies our understanding of retinal are represented. This review highlights recent function and suggest implications for future RGC: retinal ganglion cell progress on understanding the visual function work in the retina and other areas of the ner- of the retina, with emphasis in these two areas. vous system. 2 Field · Chichilnisky ANRV314-NE30-01 ARI 7 May 2007 17:2 Scope 1974a, Fukuda et al. 1984, Peichl & Wassle As in any review, brevity demands focus. We 1981, Saito 1983). Meanwhile, the anatom- ical and physiological properties of less fre- focus on the topics above because they are LGN: lateral likely to be important for understanding pri- quently observed cell types received less at- geniculate nucleus mate vision and because they have impor- tention (Cleland & Levick 1974b; see Troy tant parallels in other areas of neuroscience. & Shou 2002); some of these cell types may We also focus on studies relevant to cone- be homologous to cell types identified in the mediated (daylight) vision with an emphasis rabbit retina (e.g., Caldwell & Daw 1978b, on primate retina where possible, although Rockhill et al. 2002, Roska & Werblin 2001; results in other species (usually mammalian) see Masland 2001). are discussed as necessary. Numerous reviews, Work in primate retina followed a some- books, and chapters have been written on var- what similar path (see Shapley & Perry 1986). ious aspects of retinal structure and function, A key finding was that midget and para- including many important areas that are not sol RGCs (Rodieck et al. 1985, Watanabe covered here (Dacey 2000, 2004; Dowling & Rodieck 1989), which exhibit sustained 1987; Field et al. 2005; Lee 1996; Lukasiewicz and transient responses respectively (de 2005; Masland 2001; Meister & Berry 1999; Monasterio 1978, de Monasterio & Gouras Rodieck 1988, 1998; Sterling & Demb 2004; 1975, Gouras 1968), project to the parvocel- Taylor & Vaney 2003; Troy & Shou 2002; lular and magnocellular layers of the LGN Wassle 2004; Wassle & Boycott 1991). When- respectively (Perry et al. 1984). This and sub- ever possible, we refer to these sources for sequent findings on parvocellular and mag- background information and a more compre- nocellular projections to the visual cortex hensive list of citations. spurred investigation of the distinctions be- tween the two “pathways,” including dif- ferent spatial resolution, response dynamics, MANY DISTINCT PATHWAYS OF and chromatic properties (see Merigan & VISUAL INFORMATION Maunsell 1993, Silveira et al. 2004). The sim- EMANATE FROM THE RETINA plicity of this two-pathway model of visual processing generated great interest in its func- Background tional significance (e.g., Livingstone & Hubel Early physiological recordings from cat retina 1988). For the most part, the possibility that by 69.200.94.6 on 07/11/07. For personal use only. focused primarily on two functionally defined signals from other RGC types played a signif- types of RGCs. One type (X) summed vi- icant role in primate vision was ignored [in- sual inputs approximately linearly over space cluding cell types that project to the LGN and exhibited sustained changes in firing rate (Rodieck & Watanabe 1993)], in part because Annu. Rev. Neurosci. 2007.30:1-30. Downloaded from arjournals.annualreviews.org in response to a change in light intensity; the midget and parasol cells constitute a sub- the second type (Y) performed a more com- stantial majority (∼70%) of the entire RGC plex nonlinear computation over space and population (Dacey 2004, Perry et al. 1984). exhibited more transient responses (Cleland et al. 1971, Enroth-Cugell & Robson 1966; see Troy & Shou 2002). Anatomical work in Advances cat retina also focused primarily on two major Small bistratified cells. A major crack in the RGC types, termed alpha and beta (Boycott standard picture was the discovery of a new & Wassle 1974; see Sterling & Demb 2004). RGC type in the primate retina, the small bis- These two cell types corresponded to the X tratified cell (Figures 1, 2), which conveys a and Y cells, respectively, cementing the no- distinctive blue-on/yellow-off color signal to tion of two primary pathways in cat retina the brain (Calkins et al. 1998, Dacey & Lee (Boycott & Wassle 1974, Cleland & Levick 1994). The bistratified dendritic morphology www.annualreviews.org • Information Processing in the Retina 3 ANRV314-NE30-01 ARI 7 May 2007 17:2 PE OS Cone ONL Rod OPL Horizontal INL Bipolar Amacrine IPL GCL RGC Parasol RGC Midget RGC Small bistratified RGC Figure 1 Schematic illustration
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