Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex

Erzurumlu, Reha S.; Jhaveri, Sonal

doi:10.1016/0165-3806(90)90087-f

Cited by 195 publications

(116 citation statements)

References 26 publications

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“…By these ages, layer IV barrels and septa become evident cytoarchitecturally (Rice et al, 1985) and VPM projections are already organized into whisker-related clusters occupying barrel centers (asterisks, Fig. 8E) as expected (Erzurumlu and Jhaveri, 1990; Schlaggar and O’Leary, 1994; Catalano et al, 1996; Rhoades et al, 1996). However, labeled POm TCAs did not yet display any obvious parcellation to septa at P4; instead they traversed both barrel center and septal compartments (Fig.…”

Section: Resultssupporting

confidence: 61%

“…One idea has been that VPM afferents arrive first, forming a barrel/septa-template to which later-arriving POm TCAs conform. This is based principally on the observations that barrel centers are discernible cytoarchitecturally earlier than septa (Rice and Van der Loos, 1977) and that VPM TCAs are present within infragranular layers at birth and rapidly (within ~1–2 days) form whisker-related clusters (Wise and Jones, 1978; Erzurumlu and Jhaveri, 1990; Senft and Woolsey, 1991; Agmon et al, 1993; Schlaggar and O’Leary, 1994; Catalano et al, 1996; Rebsam et al, 2002). Our data demonstrate that POm TCAs are also well-represented within infragranular layers by birth in both rats and mice, in agreement with a previous study of POm TCAs in developing rats (Galazo et al, 2007), and exhibit single-fiber morphology and a laminar innervation pattern very similar to those reported for VPM axons (Catalano et al, 1996; Rebsam et al, 2002; Lee et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

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Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

Kichula

Huntley

2008

J of Comparative Neurology

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The thalamocortical projection to rodent barrel cortex consists of inputs from the ventral posterior medial (VPM) and posterior medial (POm) nuclei that terminate in largely non-overlapping territories in and outside of layer IV. This projection in both rats and mice has been used extensively to study development and plasticity of highly-organized synaptic circuits. Whereas the VPM pathway has been well characterized in both rats and mice, organization of the POm pathway has only been described in rats, and no studies have focused exclusively on the development of the POm projection. Here, using transport of PHA-L or carbocyanine dyes, we characterize the POm thalamocortical innervation of adult mouse barrel cortex and describe its early postnatal development in both mice and rats. In adult mice, POm inputs form a dense plexus in layer Va that extends uniformly underneath layer IV barrels and septa. Innervation of layer IV is very sparse; a clear septal innervation pattern is evident only at the layer IV/Va border. This pattern differs subtly from that described previously in rats. Developmentally, in both species, POm axons are present in barrel cortex at birth, where in mice, they occupy layer IV as it differentiates. In contrast, in rats, POm axons do not enter layer IV until 1–2 days after its emergence from the cortical plate. In both species, arbors undergo progressive and directed growth. However, no layer IV septal innervation pattern emerges until several days after the cytoarchitectonic appearance of barrels and well after the emergence of whisker-related clusters of VPM thalamocortical axons. The mature pattern resolves earlier in rats than in mice. Taken together, these data reveal anatomical differences between mice and rats in development and organization of POm inputs to barrel cortex, with implications for species differences in the nature and plasticity of lemniscal and paralemniscal information processing.

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Section: Resultssupporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

Kichula

Huntley

2008

J of Comparative Neurology

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“…1d). The barrels are consolidated during the first postnatal week through inputs from subcortical somatosensory nuclei 8,18 . We detected very little or no Cre-mediated recombination in these nuclei during this period or earlier (see Supplementary Information).…”

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confidence: 99%

“…In the CxNR1KO cortex, although cytochrome-oxidase-dense patches were organized into five rows in a similar orientation as in control animals, these patches were smaller and less distinct. Cytochrome oxidase patches that correspond to sinus hairs and digits were mostly absent.We used the lipophilic tracer, DiI, (applied to ventrobasal thalamus) 18 and serotonin transporter (5-HTT)-based immunohistochemistry 24 to visualize thalamocortical projections (n = 15 CxNR1KO, n = 17 control; both at P5). Both markers showed that thalamocortical projections displayed patches only in the large whisker representation area in the CxNR1KO mice.…”

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confidence: 99%

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Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex

Iwasato

Datwani

Wolf

et al. 2000

Nature

470

509

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In the rodent primary somatosensory cortex, the configuration of whiskers and sinus hairs on the snout and of receptor-dense zones on the paws is topographically represented as discrete modules of layer IV granule cells (barrels) and thalamocortical afferent terminals 1,2 . The role of neural activity, particularly activity mediated by NMDARs (N-methyl-D-aspartate receptors), in patterning of the somatosensory cortex has been a subject of debate [3][4][5][6] . We have generated mice in which deletion of the NMDAR1 (NR1) gene is restricted to excitatory cortical neurons, and here we show that sensory periphery-related patterns develop normally in the brainstem and thalamic somatosensory relay stations of these mice. In the somatosensory cortex, thalamocortical afferents corresponding to large whiskers form patterns and display critical period plasticity, but their patterning is not as distinct as that seen in the cortex of normal mice. Other thalamocortical patterns corresponding to sinus hairs and digits are mostly absent. The cellular aggregates known as barrels and barrel boundaries do not develop even at sites where thalamocortical afferents cluster. Our findings indicate that cortical NMDARs are essential for the aggregation of layer IV cells into barrels and for development of the full complement of thalamocortical patterns.The rodent somatosensory system is an excellent model to study molecular mechanisms underlying the establishment of patterned topographic connections between the sensory periphery and the brain. Trigeminal and dorsal column pathways convey a somatosensory map from the periphery to the neocortex by relay stations in the brainstem and the ventrobasal thalamus. At each level, pre-synaptic afferents and their target cells establish a patterned array of modules corresponding to the arrangement of whiskers and sinus hairs on the snout (trigeminal pathway), and receptor-dense zones of the paws (dorsal column pathway) 2,7,8 . These patterns are consolidated during the first postnatal week, and are subject to alterations if the sensory periphery is perturbed by nerve or whisker lesions during a critical period 2,7,8 . Thus, early neural activity might be essential in the development and plasticity of central patterns much like that of the vertebrate visual system 9,10 . Within this context, NMDAR activity has attracted much attention 9,11 . Initial studies using pharmacological blockade of NMDARs in postnatal rat somatosensory cortex did not detect effects on thalamocortical patterning, but revealed functional impairment of thalamocortical connectivity and whisker-specific responsiveness of barrel neurons 4,5 . In contrast, genetic manipulations of NMDARs showed an absence of periphery-related patterns in the somatosensory cortex 6 . This result could not be ascribed to direct effects on the neocortex, however, as it could have been a consequence of impaired patterns at the brainstem level 6,12,13 . To delineate the specific role(s) of cortical NMDARs in patterning, here we disrupted the ...

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Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex

1996

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The morphology of individual thalamocortical axons in developing rat primary somatosensory cortex was studied using lipophilic tracers. Anterograde labeling with lipophilic dyes demonstrated a topographical organization of thalamocortical projections exiting the thalamus as early as embryonic day (E) 16; retrograde labeling studies demonstrated topography of these projections as they reached the cortex as early as E18. At E17, axons course tangentially within the intermediate zone and turn or branch near the deepest layer of cortex (layer VIb), suggesting the presence of guidance cues in this region. Axons appear to grow and branch progressively within layers VIb and VIa during the following days; axons in the intermediate zone may give rise to radially directed branches. Individual axons appear to grow steadily and progressively into the cortex, with the leading front of axons at the transition zone between the cortical plate (CP) and the differentiating cortical layers. At birth (P0), thalamocortical axons extend radially through layers VIa and V and emit branches within these layers; some axons reach the CP. By P1, layer IV has begun to differentiate and axons begin to form a few simple branches in the vicinity of the layer IV cells. Over the ensuing week, axons generate more branches within layer IV, but the tangential extent of individual axon arbors does not exceed the width of a barrel. By P7, individual axons overlap within barrel clusters, and individual axons span the width of a cluster. These observations indicate that thalamic afferents develop by progressive growth of arbors that remain spatially restricted, rather than by overbranching and retracting arbors.

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Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex

Cited by 195 publications

References 26 publications

Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex

Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex

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