The formation of a cortical somatotopic map

Killackey, Herbert P.; Rhoades, Robert W.; Bennett‐Clarke, Carol A.

doi:10.1016/0166-2236(95)93937-s

Cited by 148 publications

(82 citation statements)

References 45 publications

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“…Whisker and digit-related patterns are first established in the brainstem somatosensory nuclei, then in the ventrobasal nuclear complex (VB) of the dorsal thalamus, and finally in the layer IV of the neocortex. Such cellular modules are called "barreloids" in the VB, and "barrelettes" in the brainstem (Woolsey and Van der Loos, 1970;Van der Loos, 1976;Ma and Woolsey, 1984 Van der Loos, 1986;Woolsey, 1990;O'Leary et al, 1994;Killackey et al, 1995). Several lines of evidence also indicate that somatosensory periphery-related neural maps and patterns are conveyed to target cells by the afferents at each synaptic relay station Jhaveri, 1990, 1992a, b;Senft and Woolsey, 1991).…”

Section: Indexing Termsmentioning

confidence: 99%

Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice

et al. 2005

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Development of whisker-specific neural patterns in the rodent somatosensory system requires NMDA receptor (NMDAR)-mediated activity. In cortex-specific NR1 knockout (CxNR1KO) mice, while thalamocortical afferents (TCAs) develop rudimentary whisker-specific patterns in the primary somatosensory (barrel) cortex, layer IV cells do not develop barrels or orient their dendrites towards TCAs. To determine the role of postsynaptic NMDARs in presynaptic afferent development and patterning in the barrel cortex, we examined the single TCA arbors in CxNR1KO mice between postnatal days (P) 1-7. Sparsely branched TCAs invade the cortical plate on P1 in CxNR1KO mice as in control mice. In control animals, TCAs progressively elaborate patchy terminals, mostly restricted to layer IV. In CxNR1KO mice, TCAs develop far more extensive arbors between P3-7. Their lateral extent is twice that of controls from P3 onwards. By P7, CxNR1KO TCAs have significantly fewer branch points and terminal endings in layers IV and VI but more in layers II/III and V than control mouse TCAs. Within expansive terminal arbors, CxNR1KO TCAs develop focal terminal densities in layer IV, corresponding to the rudimentary whisker-specific patches. Given that thalamic NMDARs are spared in CxNR1KO mice, the present results show that postsynaptic NMDARs play an important role in refinement of presynaptic afferent arbors and whisker-specific patterning in the developing barrel cortex. Indexing termsbarrels; barreloids; trigeminal system; somatosensory cortex; region-specific gene knockout A conspicuous feature of the rodent primary somatosensory cortex is the presence of neural patterns within face and digit representation regions of the body map. Patches of thalamocortical afferent (TCA) arbors and their postsynaptic partners form discrete modules that replicate the patterned distribution of whiskers on the contralateral snout. These cellular modules are termed "barrels" (Woolsey and Van der Loos, 1970). Whisker and digit-related patterns are first established in the brainstem somatosensory nuclei, then in the ventrobasal nuclear complex (VB) of the dorsal thalamus, and finally in the layer IV of the neocortex. Such cellular modules are called "barreloids" in the VB, and "barrelettes" in the brainstem (Woolsey and Van der Loos, 1970;Van der Loos, 1976;Ma and Woolsey, 1984 Van der Loos, 1986;Woolsey, 1990;O'Leary et al., 1994;Killackey et al., 1995). Several lines of evidence also indicate that somatosensory periphery-related neural maps and patterns are conveyed to target cells by the afferents at each synaptic relay station Jhaveri, 1990, 1992a, b;Senft and Woolsey, 1991).In recent years, a number of transgenic and knockout (KO) mouse models have begun yielding clues to the underlying mechanisms of pattern formation in the rodent somatosensory system, with profound implications for other sensory pathways in the mammalian brain. Current understanding is that topographically organized projections (somatotopic maps) along the somatosensory system are es...

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Section: Indexing Termsmentioning

confidence: 99%

Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice

et al. 2005

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“…Patterned cortical maps (barrel fields) are established during a critical period in development and depend on an intact sensory periphery and subcortical somatosensory structures (Killackey et al, 1995;O'Leary et al, 1994;Woolsey, 1990). Whisker and digit-related patterns are first established in the brainstem somatosensory nuclei, then in the VPM-VPL complex of the dorsal thalamus and finally in the neocortex (Belford and Killackey, 1980;Ma and Woolsey, 1984;Van der Loos, 1976;Woolsey and Van der Loos, 1970).…”

mentioning

confidence: 99%

“…Whisker and digit-related patterns are first established in the brainstem somatosensory nuclei, then in the VPM-VPL complex of the dorsal thalamus and finally in the neocortex (Belford and Killackey, 1980;Ma and Woolsey, 1984;Van der Loos, 1976;Woolsey and Van der Loos, 1970). The instructive role of the sensory periphery in sculpting central neural patterns has been demonstrated by whisker follicle or trigeminal nerve lesion studies performed in perinatal rodents, or in mice selectively bred for aberrant numbers of whiskers (Killackey et al, 1995;O'Leary et al, 1994;Welker and Van der Loos, 1986;Woolsey, 1990). Several lines of evidence indicate that somatosensory periphery-related neural maps and patterns are conveyed to target cells by the afferents at each synaptic relay station Jhaveri, 1990, 1992a,b;Erzurumlu and Killackey, 1983;Senft and Woolsey, 1991).…”

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confidence: 99%

Somatosensory cortical plasticity: recruiting silenced barrels by active whiskers

Erzurumlu

2003

Experimental Neurology

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“…O ne prominent characteristic of the rodent whisker-somatosensory system is its precisely organized topographic sensory maps (1)(2)(3). Each whisker is innervated by peripheral axons of a subset of trigeminal sensory neurons whose cell bodies reside in the trigeminal ganglia (TG) and central axons project to the brainstem (4).…”

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confidence: 99%

Proper formation of whisker barrelettes requires periphery-derived Smad4-dependent TGF-β signaling

Silva

Hasegawa

Scott

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Mammalian somatosensory topographic maps contain specialized neuronal structures that precisely recapitulate the spatial pattern of peripheral sensory organs. In the mouse, whiskers are orderly mapped onto several brainstem nuclei as a set of modular structures termed barrelettes. Using a dual-color iontophoretic labeling strategy, we found that the precise topography of barrelettes is not a result of ordered positions of sensory neurons within the ganglion. We next explored another possibility that formation of the whisker map is influenced by periphery-derived mechanisms. During the period of peripheral sensory innervation, several TGF-β ligands are exclusively expressed in whisker follicles in a dynamic spatiotemporal pattern. Disrupting TGF-β signaling, specifically in sensory neurons by conditional deletion of Smad4 at the late embryonic stage, results in the formation of abnormal barrelettes in the principalis and interpolaris brainstem nuclei and a complete absence of barrelettes in the caudalis nucleus. We further show that this phenotype is not derived from defective peripheral innervation or central axon outgrowth but is attributable to the misprojection and deficient segregation of trigeminal axonal collaterals into proper barrelettes. Furthermore, Smad4-deficient neurons develop simpler terminal arbors and form fewer synapses. Together, our findings substantiate the involvement of whisker-derived TGF-β/Smad4 signaling in the formation of the whisker somatotopic maps.O ne prominent characteristic of the rodent whisker-somatosensory system is its precisely organized topographic sensory maps (1-3). Each whisker is innervated by peripheral axons of a subset of trigeminal sensory neurons whose cell bodies reside in the trigeminal ganglia (TG) and central axons project to the brainstem (4). Sensory afferents carrying information from individual whiskers segregate and converge to form modular structures termed barrelettes, whose spatial organization exactly mirrors that of the whiskers in the periphery (5). The barrelette map in the brainstem emerges during development and serves as a template for the subsequent generation of homologous upstream structures in the thalamus and cortex, termed barreloids and barrels, respectively (5, 6). Interestingly, induction of an extra whisker by exogenous expression of Shh during early development leads to the formation of an extra barrelette with a topographic position corresponding to that of the ectopic whisker (7). Together with other studies (8-10), these data suggest that the formation of the whisker map is under the strong instructive influence of the periphery. The whisker-derived signals regulating barrelette formation remain mostly unknown, however.Previous work showed that BMP4 signaling induces differential expression of genes in trigeminal sensory neurons innervating different areas of the face along the dorsoventral axis (11,12). At later developmental stages, multiple TGF-β superfamily ligands are expressed in whisker follicles during the period of sensory...

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The formation of a cortical somatotopic map

Cited by 148 publications

References 45 publications

Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice

Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice

Somatosensory cortical plasticity: recruiting silenced barrels by active whiskers

Proper formation of whisker barrelettes requires periphery-derived Smad4-dependent TGF-β signaling

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