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Mechanisms underlying development of visual maps and receptive fields - PubMed

Review

Mechanisms underlying development of visual maps and receptive fields

Andrew D Huberman et al. Annu Rev Neurosci. 2008.

Abstract

Patterns of synaptic connections in the visual system are remarkably precise. These connections dictate the receptive field properties of individual visual neurons and ultimately determine the quality of visual perception. Spontaneous neural activity is necessary for the development of various receptive field properties and visual feature maps. In recent years, attention has shifted to understanding the mechanisms by which spontaneous activity in the developing retina, lateral geniculate nucleus, and visual cortex instruct the axonal and dendritic refinements that give rise to orderly connections in the visual system. Axon guidance cues and a growing list of other molecules, including immune system factors, have also recently been implicated in visual circuit wiring. A major goal now is to determine how these molecules cooperate with spontaneous and visually evoked activity to give rise to the circuits underlying precise receptive field tuning and orderly visual maps.

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Figures

Figure 1
Figure 1

Timing of the development of each of the major visual circuit properties in ferret and mouse (shown as bars with light blue gradients). Orange bars indicate ionotropic glutamate receptor-mediated retinal waves. Turquoise bars indicate nicotinic acetylcholine receptor–mediated retinal waves. Blue bars (stage I waves) indicate cholinergic and gap-junction-mediated activity. Gray column indicates the approximate age for eye opening in each species. Black icons within the “visually-evoked activity” yellow bar indicates the period in which vision occurs through naturally closed eye lids. White icons indicate vision through open eyelids. Asterisks in the two bars labeled “ODCs” indicate that two different time frames have been reported for ODC development in ferrets (early development of ODCs, Crowley & Katz 2000; later development of ODCs, Ruthazer et al. 1999) and which report is accurate remains controversial owing to technical limitations of the tracing techniques used in both studies (see main text). Note that ODCs, orientation maps, and direction maps are not listed for the mouse because mice lack these anatomical features, although single cells in mouse V1 do exhibit responses tuned according to these stimulus features. The timing of the emergence of these physiological features in the mouse has not yet been reported.

Figure 2
Figure 2

Schematic diagrams of the types of molecular cues that direct wiring specificity in developing visual circuits. (a) Graded expression of guidance cues in axons and in their targets can guide specific patterns of visual connections according to matching of ligand and receptor levels (see reviews by McLaughlin & O’Leary 2005, Flanagan 2006) and see Figure 3. (b) Homophilic adhesion cues expressed in the axons and dendrites of pre- and postsynaptic neurons can lead to highly specific patterns of connectivity (red cells connect to red cells, green cells to green cells, etc.) (e.g., Yamagata et al. 2002). Similarly, the expression of adhesion molecules in neurons within one structure (shown in blue; schematic of the mouse LGN) and within the specific layer of their targets to which they project (also shown in blue; schematic of cortex) can induce highly specific patterns of connectivity (e.g., Poskanzer et al. 2003). (c) Adhesive cues expressed among axons arising from a common cell type (schematized here as red, green or yellow) can segregate these axons into distinct fiber tracts and/or portions of fiber tracts, which can then lead to segregation of their axons within the final target (reviewed in Chen & Flanagan 2006, Mombaerts 2006). (d ) Different adhesion cues expressed at different sites along the dendritic arbor of an individual postsynaptic neuron can segregate synaptic inputs arising from different cells/sources at the subcellular level (e.g., Ango et al. 2004, Di Cristo et al. 2004) and thereby impact the receptive field properties of the postsynaptic neuron (e.g., Sherman 2004).

Figure 3
Figure 3

Schematic diagrams of (a) the mature retinotopic map in the SC, (b) the immature unrefined retinotopic map in the SC (and the expression of molecular cues that guide formation of retinotopic maps) (see McLaughlin & O’Leary 2005). (c) Disruptions in retinotopic mapping in ephrin-A2/5−/− or EphA5−/− mice. Multiple dense termination zones are observed along the N-T axis of the target (Feldheim et al. 2000, 2004). Waves denote that retinal waves are intact in these animals. (d ) Disruptions in retinotopic mapping in EphB2/3−/− mice or in response to disrupting Wnt/ryk signaling; RGC terminals shift more medially (ryk disruption; dashed lines in target) (Schmitt et al. 2006) or shift more laterally (EphB2/3 knockout; solid lines) (Hindges et al. 2002). Similar results are observed after disruption of BMPs (Chandrasekaran et al. 2005). (e) The overall retinotopic map forms when stage II retinal waves are eliminated (because ephrin-A2/5 signaling is still intact), but RGC axons fail to form dense terminal arbors in their correct topopographic locations and are abnormally broad (McLaughlin et al. 2003, Grubb et al. 2003). (f )When stage II waves are prevented in ephrin-A2/5−/− mice, N-T mapping of RGC projections is abolished (Pfeiffenberger et al. 2006). For all the manipulations shown here, the retino-SC projection is depicted. The same general defect pattern is observed in the LGN and V1, where ephrin-As and Bs and retinal waves regulate topographic map formation (see main text for details).

Figure 4
Figure 4

Schematic representations of the eye-specific projection patterns to the LGN of the ferret (panels a– j ) and the mouse (panels k–t) during normal development and the results of experiments examining the role of spontaneous retinal activity, ephrin-As, and immune genes in eye-specific retino-LGN segregation. (b, l ) The early prerefined pattern of RGC inputs to the LGN in the newborn ferret (b) and mouse (l ). Red areas of the LGN correspond to territory occupied by RGC axons arising from the right (red ) eye, and green areas correspond the territory occupied by RGC axons from the left (green) eye. Yellow corresponds to the LGN territory where red and green axons from the two eyes overlap. The ages depicted are shown in parentheses. The manipulations leading to each phenotype are described in each box, as well as in the main text. The asterisk above *NP1/2 and * P25 in panel t refers to the fact that the lack of eye-specific segregation observed in the P10 NP1/2−/− mouse changes to a pattern similar to panel p by P25. By contrast, C1q−/− mice and MHCI−/− mice exhibit defects in eye-specific segregation until at least P25.

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