Vision and Cortical Map Development
2007; Cell Press; Volume: 56; Issue: 2 Linguagem: Inglês
10.1016/j.neuron.2007.10.011
ISSN1097-4199
AutoresLeonard White, David Fitzpatrick,
Tópico(s)Neuroscience and Neuropharmacology Research
ResumoFunctional maps arise in developing visual cortex as response selectivities become organized into columnar patterns of population activity. Recent studies of developing orientation and direction maps indicate that both are sensitive to visual experience, but not to the same degree or duration. Direction maps have a greater dependence on early vision, while orientation maps remain sensitive to experience for a longer period of cortical maturation. There is also a darker side to experience: abnormal vision through closed lids produces severe impairments in neuronal selectivity, rendering these maps nearly undetectable. Thus, the rules that govern their formation and the construction of the underlying neural circuits are modulated—for better or worse—by early vision. Direction maps, and possibly maps of other properties that are dependent upon precise conjunctions of spatial and temporal signals, are most susceptible to the potential benefits and maladaptive consequences of early sensory experience. Functional maps arise in developing visual cortex as response selectivities become organized into columnar patterns of population activity. Recent studies of developing orientation and direction maps indicate that both are sensitive to visual experience, but not to the same degree or duration. Direction maps have a greater dependence on early vision, while orientation maps remain sensitive to experience for a longer period of cortical maturation. There is also a darker side to experience: abnormal vision through closed lids produces severe impairments in neuronal selectivity, rendering these maps nearly undetectable. Thus, the rules that govern their formation and the construction of the underlying neural circuits are modulated—for better or worse—by early vision. Direction maps, and possibly maps of other properties that are dependent upon precise conjunctions of spatial and temporal signals, are most susceptible to the potential benefits and maladaptive consequences of early sensory experience. The information necessary to represent visual scenes resides in the spatial and temporal properties of a distributed pattern of neural activity in the primary visual cortex (V1). This activity arises from the aggregate responses of individual neurons that are differentially tuned to features of visual stimuli, such as their position in visual space and the energy engendered by their orientation, spatial frequency, and direction of motion. For carnivores and primates, neurons with similar preferences are clustered into radial columns, which are arrayed in a systematic fashion across the cortical surface. This arrangement of response preferences in V1 into so-called functional maps was first recognized nearly 50 years ago in the seminal work of D.H. Hubel and T.N. Wiesel, who probed the organization of visual cortex with microelectrodes and neuroanatomical tracers (see Hubel and Wiesel, 2005Hubel D.H. Wiesel T.N. Brain and Visual Perception. Oxford University Press, New York2005Google Scholar). In the last two decades, it has become possible to use optical means for measuring signals (either intrinsic or exogenous) that indirectly reflect underlying neuronal selectivities and preferences and thereby characterize the spatial layout of functional maps across the accessible reaches of the visual cortex (usually the representation of central visual space in V1 and/or V2 of model carnivore and primate species) (Blasdel and Salama, 1986Blasdel G.G. Salama G. Voltage-sensitive dyes reveal a modular organization in monkey striate cortex.Nature. 1986; 321: 579-585Crossref PubMed Scopus (584) Google Scholar, Bonhoeffer and Grinvald, 1996Bonhoeffer T. Grinvald A. Optical imaging based on intrinsic signals: the methodology.in: Toga A.W. Mazziotta J.C. Brain Mapping: The Methods. Academic Press, San Diego, CA1996: 55-97Google Scholar). Based largely on the results of such imaging studies of population activity in V1, numerous functional maps have been proposed to account for the spatial organization of coherent population activity in V1 (Bonhoeffer and Grinvald, 1991Bonhoeffer T. Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns.Nature. 1991; 353: 429-431Crossref PubMed Scopus (622) Google Scholar, Shmuel and Grinvald, 1996Shmuel A. Grinvald A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18.J. 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We find it useful to categorize these functional maps into one of two groups: (1) maps that recapitulate the topological (near-neighbor) relations established in the lateral geniculate nucleus; and (2) maps that represent functional properties that emerge from geniculocortical interactions and intracortical processing. In the first category are the retinotopic (visuotopic) map and the ocular-dominance map, both of which are established in layer 4—the principal thalamic recipient layer—and organized to accommodate the two sets of monocular inputs that arise from the principal layers of the lateral geniculate nucleus. Maps in the second category do not simply reflect the neuronal properties and spatial patterns of organization that are established in antecedent levels of the visual pathway. The best example in this category is the map of orientation preference, a columnar map of a neuronal response property that is elaborated with a high degree of selectivity in the visual cortex, but not in the lateral geniculate nucleus (Hubel and Wiesel, 1962Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154PubMed Google Scholar, Hubel and Wiesel, 1968Hubel D.H. Wiesel T.N. Receptive fields and functional architecture of monkey striate cortex.J. Physiol. 1968; 195: 215-243PubMed Google Scholar, Swindale et al., 1987Swindale N.V. Matsubara J.A. Cynader M.S. Surface organization of orientation and direction selectivity in cat area 18.J. Neurosci. 1987; 7: 1414-1427PubMed Google Scholar, Bonhoeffer and Grinvald, 1991Bonhoeffer T. Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns.Nature. 1991; 353: 429-431Crossref PubMed Scopus (622) Google Scholar). Orientation-preference maps in V1 of carnivores and primates are characterized by numerous iterations of pinwheel motifs and linear zones that represent orientation preference in a smooth and continuous fashion across the surface of V1, save for point discontinuities at pinwheel centers (Bonhoeffer and Grinvald, 1991Bonhoeffer T. Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns.Nature. 1991; 353: 429-431Crossref PubMed Scopus (622) Google Scholar, Bosking et al., 1997Bosking W.H. Zhang Y. Schofield B. Fitzpatrick D. Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex.J. Neurosci. 1997; 17: 2112-2127PubMed Google Scholar, Blasdel, 1992Blasdel G.G. Orientation selectivity, preference, and continuity in monkey striate cortex.J. 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Cortical cartography revisited: a frequency perspective on the functional architecture of visual cortex.Prog. Brain Res. 2006; 154: 121-134Crossref PubMed Scopus (20) Google Scholar). Another member of this second category is the map of direction preference, which is present in V1 in carnivores and in middle temporal visual areas in primates (Albright, 1984Albright T.D. Direction and orientation selectivity of neurons in visual area MT of the macaque.J. Neurophysiol. 1984; 52: 1106-1130PubMed Google Scholar, Malonek et al., 1994Malonek D. Tootell R.B. Grinvald A. Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT.Proc. R. Soc. Lond. B. Biol. Sci. 1994; 258: 109-119Crossref Scopus (127) Google Scholar, Shmuel and Grinvald, 1996Shmuel A. Grinvald A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18.J. 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USA. 2004; 101: 2566-2571Crossref PubMed Scopus (27) Google Scholar). The map of direction preference is nested geometrically within the map of orientation preference, such that each iso-orientation domain is subdivided into a pair of smaller domains that represent opposite directions of stimulus motion (Shmuel and Grinvald, 1996Shmuel A. Grinvald A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18.J. Neurosci. 1996; 16: 6945-6964PubMed Google Scholar, Weliky et al., 1996Weliky M. Bosking W.H. Fitzpatrick D. A systematic map of direction preference in primary visual cortex.Nature. 1996; 379: 725-728Crossref PubMed Scopus (190) Google Scholar, Kisvárday et al., 2001Kisvárday Z.F. Buzás P. Eysel U.T. Calculating direction maps from intrinsic signals revealed by optical imaging.Cereb. Cortex. 2001; 11: 636-647Crossref PubMed Scopus (25) Google Scholar). While the functional significance of cortical maps continues to be a subject of debate (see, e.g., Chklovskii and Koulakov, 2004Chklovskii D.B. Koulakov A.A. Maps in the brain: what can we learn from them?.Annu. Rev. Neurosci. 2004; 27: 369-392Crossref PubMed Scopus (246) Google Scholar, Swindale, 2000Swindale N.V. How many maps are there in visual cortex?.Cereb. Cortex. 2000; 10: 633-643Crossref PubMed Scopus (69) Google Scholar, Horton and Adams, 2005Horton J.C. Adams D.L. The cortical column: a structure without a function.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005; 360: 837-862Crossref PubMed Scopus (342) Google Scholar), they have served as useful models for exploring the mechanisms responsible for the development of neuronal response properties in V1 and the neural circuits from which they arise. These mechanisms can be divided into two basic classes: (1) molecular recognition mechanisms that rely on gradients of diffusible ligands and cell-surface receptors to specify map topology and (2) activity-dependent mechanisms that rely on correlated patterns of pre- and postsynaptic activity to guide map formation. The latter can be further refined according to the source of the neural activity patterns: activity that arises endogenously within the developing retino-geniculo-cortical network and—at later times in development—activity that is driven by visual experience. Undoubtedly, a finely tuned orchestration of all of these mechanisms is essential for the proper establishment and subsequent maturation of functional cortical maps. This is best exemplified by the development of the map of visual space in the tectum, where the mechanisms are best understood (for reviews, see Goodhill and Xu, 2005Goodhill G.J. Xu J. The development of retinotectal maps: a review of models based on molecular gradient.Network. 2005; 16: 5-34Crossref PubMed Scopus (43) Google Scholar, Lemke and Reber, 2005Lemke G. Reber M. Retinotopic mapping: new insights from molecular genetics.Annu. Rev. Cell Dev. Biol. 2005; 21: 551-580Crossref PubMed Scopus (84) Google Scholar, O'Leary and McLaughlin, 2005O'Leary D.D.M. McLaughlin T. Mechanisms of retinotopic map development: Ephs, ephrins, and spontaneous correlated retinal activity.Prog. Brain Res. 2005; 147: 43-65Crossref PubMed Scopus (81) Google Scholar). The initial formation of this map depends on molecular gradients that insure the guidance of axons to the topologically appropriate portions of the map; similar molecular mechanisms are likely to operate in V1 (Cang et al., 2005Cang J. Kaneko M. Yamada J. Woods G. Stryker M.P. Feldheim D.A. Ephrin-As guide the formation of functional maps in the visual cortex.Neuron. 2005; 48: 577-589Abstract Full Text Full Text PDF PubMed Scopus (135) Google Scholar). But such mechanisms provide only course instruction of map topology; at later stages in development, patterns of retinal activity are required to achieve the finely tuned precision that is characteristic of the mature map. The precise role of molecular recognition mechanisms in the formation of other cortical maps remains unclear (Crowley and Katz, 2002Crowley J.C. Katz L.C. Ocular dominance development revisited.Curr. Opin. Neurobiol. 2002; 12: 104-109Crossref PubMed Scopus (78) Google Scholar; Huberman et al., 2006Huberman A.D. Speer C.M. Chapman B. Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1.Neuron. 2006; 52: 247-254Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar); but a similar sequence—an initial stage that specifies the basic structure of the map, followed by a subsequent stage of map refinement—is generally thought to account for the development of all cortical maps. Furthermore, because the maps of visual space and ocular dominance are fully evident before birth in primates and before the postnatal separation of the eyelids in carnivores, the formative stages of these maps occur in the absence of patterned visual experience. Sensory experience does alter the structure of these maps when input from the two eyes is rendered unbalanced, as has been shown repeatedly for the map of ocular dominance and more recently for the retinotopic map (Smith and Trachtenberg, 2007Smith S.L. Trachtenberg J.T. Experience-dependent binocular competition in the visual cortex begins at eye opening.Nat. Neurosci. 2007; 10: 370-375Crossref PubMed Scopus (100) Google Scholar), but this is after their initial formation and early progression toward functional maturity (for recent reviews of critical period plasticity, see Knudsen, 2004Knudsen E.I. Sensitive periods in the development of the brain and behavior.J. Cogn. Neurosci. 2004; 16: 1412-1425Crossref PubMed Scopus (791) Google Scholar, Hensch, 2005Hensch T.K. Critical period plasticity in local cortical circuits.Nat. Rev. Neurosci. 2005; 6: 877-888Crossref PubMed Scopus (1405) Google Scholar, Sengpiel, 2005Sengpiel F. Visual cortex: overcoming a no-go for plasticity.Curr. Biol. 2005; 15: R1000-R1002Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar, Taha and Stryker, 2005Taha S.A. Stryker M.P. Molecular substrates of plasticity in the developing visual cortex.Prog. Brain Res. 2005; 147: 101-114Crossref Scopus (24) Google Scholar). Similarly, the experience-dependent plasticity of orientation maps, which is evident when the visual experience of juvenile animals is restricted to a narrow range of stimulus orientations, is thought to reflect the plastic potential of the map that persists for some time after its formation (Sengpiel et al., 1999Sengpiel F. Stawinski P. Bonhoeffer T. Influence of experience on orientation maps in cat visual cortex.Nat. Neurosci. 1999; 2: 727-732Crossref PubMed Scopus (150) Google Scholar, Tanaka et al., 2006Tanaka S. Ribot J. Imamura K. Tani T. Orientation-restricted continuous visual exposure induces marked reorganization of orientation maps in early life.Neuroimage. 2006; 30: 462-477Crossref PubMed Scopus (38) Google Scholar). Our purpose here is to review recent evidence suggesting that visual experience plays a more substantial role in the earlier, formative stages of orientation and direction preference map development than would have been predicted based on studies of topological maps. We will focus on the natural history of visual cortical development in the ferret, a species that has become widely used for studies of visual system development and the organization of functional maps in visual cortex, and we will discuss lessons learned from studies that have sought to manipulate the impact of vision on the formation and maturation of orientation and direction maps. A survey of recent work in this field will show that visual experience may have a profoundly beneficial or detrimental influence over the formation of these maps in the developing visual cortex. Recognition of this conclusion should impact our understanding of cortical development and the rules that govern the construction of functional maps. Understanding these rules is essential for guiding interventional efforts aimed at mitigating the central impact of abnormal experience filtered through malformed or diseased sensory organs and promoting the benefits of optimal sensory-evoked patterns of neural activity in developing cortical networks. The distinction of two phases of map development has served as a useful means of recognizing an early, experience-independent establishment phase and a subsequent refinement phase during which experience acts to shape map properties. This framework implies that most of the information that is required for map construction—establishing the basic layout of the map and determining which regions will express a particular preference—is innate and that sensory experience plays only a modest role in elaborating a program that has been largely determined by experience-independent mechanisms. It is worth keeping in mind, however, that at the time when light activation of the retina first becomes effective in driving visual cortical activity, the density of cortical synapses in V1 is only a fraction of that found in maturity, and that the vast majority of cortical synapses are added during a phase of development when visual experience impacts the spatial and temporal patterns of neural activity in V1. Indeed, the onset of visual experience—at birth in primates and eye opening in carnivores—coincides with an explosive increase in the density of cortical synapses in all cortical layers, including the supragranular layers from which emergent maps in V1 are detected. In rhesus monkey V1, for example, this phase of rapid synaptogenesis ensues late in the third trimester before birth and continues exponentially over the first two postnatal months before achieving a stable density of synaptic profiles in neuropil by the third month that persists until adolescence (Bourgeois and Rakic, 1993Bourgeois J.-P. Rakic P. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage.J. Neurosci. 1993; 13: 2801-2820Crossref PubMed Google Scholar). In carnivores, which open their eyelids some time after birth (after the first postnatal week in cat and after the fourth week in ferret), a similar phenomenon has been documented: the density of synapses in V1 increases rapidly in the month that follows the onset of patterned visual experience (Cragg, 1975Cragg B.G. The development of synapses in the visual system of the cat.J. Comp. Neurol. 1975; 160: 147-166Crossref PubMed Scopus (376) Google Scholar, Erisir and Harris, 2003Erisir A. Harris J.L. Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4.J. Neurosci. 2003; 23: 5208-5218PubMed Google Scholar). This explosive increase in V1 synaptogenesis is accompanied by a comparable increase in the outgrowth of intrinsic axonal projections in V1. Thus, the long-range horizontal connections in layer 2/3 that are known to establish connections among cortical columns with similar response properties (Gilbert and Wiesel, 1989Gilbert C.D. Wiesel T.N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex.J. Neurosci. 1989; 9: 2432-2442PubMed Google Scholar, Malach et al., 1993Malach R. Amir Y. Harel M. Grinvald A. Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex.Proc. Natl. Acad. Sci. USA. 1993; 90: 10469-10473Crossref PubMed Scopus (439) Google Scholar, Bosking et al., 1997Bosking W.H. Zhang Y. Schofield B. Fitzpatrick D. Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex.J. 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For example, at about the time of eye opening in ferret visual cortex, horizontal connections are modest, with considerably less spatial extent of coverage across the cortical surface and a lower degree of clustering than are ultimately achieved in maturity (Durack and Katz, 1996Durack J.C. Katz L.C. Development of horizontal projections in layer 2/3 of ferret visual cortex.Cereb. Cortex. 1996; 6: 178-183Crossref PubMed Scopus (79) Google Scholar, Ruthazer and Stryker, 1996Ruthazer E.S. Stryker M.P. The role of activity in the development of long-range horizontal connections in area 17 of the ferret.J. Neurosci. 1996; 16: 7253-7269PubMed Google Scholar). Adult-like distributions of intrinsic connections are achieved at about the same time in postnatal development that the rate of synaptogenesis begins to decline and synaptic densities in layer 2/3 of V1 reach a stable level. Figure 1 illustrates this point by showing representative reconstructions of horizontal connections in layer 2/3 from developing ferret visual cortex, labeled with extracellular injections of an anterograde axonal tracer (White et al., 2001White L.E. Coppola D.M. Fitzpatrick D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex.Nature. 2001; 411: 1049-1052Crossref PubMed Scopus (168) Google Scholar), plotted together with a schematic representation of synaptic density (black curve) also obtained from layer 2/3 of ferret V1 (Erisir and Harris, 2003Erisir A. Harris J.L. Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4.J. Neurosci. 2003; 23: 5208-5218PubMed Google Scholar). Although studies of developing horizontal connections in V1 have often emphasized regressive phenomenon, such as collateral pruning and selective synapse elimination as important means of achieving functional maturity, the sculpting of intrinsic cortical connectivity occurs in a larger context of net circuit construction (Purves et al., 1996Purves D. White L.E. Riddle D.R. Is neural development darwinian?.Trends Neurosci. 1996; 19: 1-8Abstract Full Text PDF PubMed Scopus (14) Google Scholar). Taken together, these neuroanatomical observations indicate that the construction of neural circuits in supragranular layers of V1 is largely accomplished during a period of time in which these circuits are responsive to patterned visual experience. Furthermore, as shown in Figure 2, this phase of rapid circuit construction ensues just as the first detectable mapping signals reveal the presence of a map of orientation preference in V1. Thus, maps of orientation are recognizable—although often not homogenous in columnar structure or signal strength—at the time of eye opening in ferret kits (Chapman et al., 1996Chapman B. Stryker M.P. Bonhoeffer T. Development of orientation-preference maps in ferret primary visual cortex.J. Neurosci. 1996; 16: 6443-6453PubMed Google Scholar, White et al., 2001White L.E. Coppola D.M. Fitzpatrick D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex.Nature. 2001; 411: 1049-1052Crossref PubMed Scopus (168) Google Scholar, Coppola and White, 2004Coppola D.M. White L.E. Visual experience promotes the isotropic representation of orientation preference.Vis. Neurosci. 2004; 21: 39-51Crossref PubMed Scopus (23) Google Scholar). Thereafter, columnar structure becomes more uniform across the cortical map and the strength of the mapping signals increases substantially before achieving functional maturity approximately three weeks after eye opening (see Figure 2, blue squares; see also Chapman et al., 1996Chapman B. Stryker M.P. Bonhoeffer T. Development of orientation-preference maps in ferret primary visual cortex.J. Neurosci. 1996; 16: 6443-6453PubMed Google Scholar, White et al., 2001White L.E. Coppola D.M. Fitzpatrick D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex.Nature. 2001; 411: 1049-1052Crossref PubMed Scopus (168) Google Scholar, Li et al., 2006Li Y. Fitzpatrick D. White L.E. The development of direction selectivity in ferret visual cortex requires early visual experience.Nat. Neurosci. 2006; 9: 676-681Crossref PubMed Scopus (131) Google Scholar). This process, as documented with intrinsic signal optical imaging techniques, parallels (with a several day lag) the maturation of neuronal orientation selectivity assessed electrophysiologically (Chapman and Stryker, 1993Chapman B. Stryker M.P. Development of orientation selectivity in ferret visual cortex and effects of deprivation.J. Neurosci. 1993; 13: 5251-5262PubMed Google Scholar, Chapman et al., 1996Chapman B. Stryker M.P. Bonhoeffer T. Development of orientation-preference maps in ferret primary visual cortex.J. Neurosci. 1996; 16: 6443-6453PubMed Google Scholar; see also Gödecke et al., 1997Gödecke I. Kim D.S. Bonhoeffer T. Singer W. Development of orientation-preference maps in area 18 of kitten visual cortex.Eur. J. Neurosci. 1997; 9: 1754-1762Crossref PubMed Scopus (64) Google Scholar). The period of postnatal cortical maturation that is characterized by the rapid construction of neural circuits in supragranular layers of V1, therefore, coincides with the phase of emergent map development when neuronal selectivities sharpen, map structures become more robust, and the mature configuration of the map is achieved (cf. Figure 1, Figure 2). In contrast to the early experience-independent formation of visual space and ocular-dominance maps, orientation maps arise during a time when visual experience has the potential to supervise the progression and outcome of circuit construction. Interestingly, this traj
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