Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Comparative Study
. 1999 Jun 1;19(11):4388-406.
doi: 10.1523/JNEUROSCI.19-11-04388.1999.

Anatomical correlates of functional plasticity in mouse visual cortex

A Antonini  1 , M Fagiolini, M P Stryker
Affiliations
Comparative Study

Anatomical correlates of functional plasticity in mouse visual cortex

A Antonini et al. J Neurosci. .

Abstract

Much of what is known about activity-dependent plasticity comes from studies of the primary visual cortex and its inputs in higher mammals, but the molecular bases remain largely unknown. Similar functional plasticity takes place during a critical period in the visual cortex of the mouse, an animal in which genetic experiments can readily be performed to investigate the underlying molecular and cellular events. The experiments of this paper were directed toward understanding whether anatomical changes accompany functional plasticity in the developing visual cortex of the mouse, as they do in higher mammals. In normal mice, transneuronal label after an eye injection clearly delineated the monocular and binocular zones of area 17. Intrinsic signal optical imaging also showed monocular and binocular zones of area 17 but revealed no finer organization of ocular dominance or orientation selectivity. In normal animals, single geniculocortical afferents serving the contralateral eye showed great heterogeneity and no clustering consistent with the presence of ocular dominance patches. Growth and elaboration of terminal arbor continues beyond postnatal day 40 (P40), after the peak of the critical period. After prolonged monocular deprivation (MD) from P20 to P60, transneuronal labeling showed that the projection serving the ipsilateral eye was severely affected, whereas the effect on the contralateral eye's pathway was inconsistent. Optical imaging also showed profound effects of deprivation, particularly in the ipsilateral pathway, and microelectrode studies confirmed continued functional plasticity past P40. Reconstruction of single afferents showed that MD from P20 to P40 promoted the growth of the open eye's geniculocortical connections without causing the closed eye's contralateral projection to shrink, whereas MD from P20 to P60 caused an arrest of growth of deprived arbors. Our findings reveal numerous similarities between mouse and higher mammals in development and plasticity, along with some differences. We discuss the factors that may be responsible for these differences.

PubMed Disclaimer

Figures

Fig. 1.
Fig. 1.
A, C,E, Consecutive 50 μm sections through the posterior pole of the cerebral hemisphere. B, D,F, Consecutive sections from the opposite hemisphere of the same mouse in which an electrolytic lesion (red arrow) was made after electrophysiological recordings to mark the border between areas 17 and 18a. Area 17 is recognizable in Nissl staining by the presence of small granule cells in layer IV (A, black arrow). High acetylcholinesterase activity in layer IV is also a marker for the primary visual cortex (C, D, light staining), as is the pattern of myelin staining (E, F). The medial border of the visual cortex is clearly identified in all three stains (arrowhead). Furthermore, there is a good match between the 17–18a border recognized in the three stains and that identified electrophysiologically (B, D, F). The pair of arrows on the left point to the binocular portion of the visual cortex clearly recognizable in all three preparations.
Fig. 2.
Fig. 2.
Extent of the mouse visual cortex in the coronal plane, as demonstrated by the transneuronal transport of WGA-HRP injected into one eye. The series of coronal sections through the hemispheres contralateral and ipsilateral to the eye injected with WGA-HRP are presented from posterior to anterior; the distance from the posterior edge of the hemispheres is indicated on theleft. The images have been obtained by scanning the photographic negatives of the histological sections. The light intensity and contrast of the images of the ipsilateral hemisphere (right column) have been enhanced to better visualize the ipsilateral projections.
Fig. 3.
Fig. 3.
Aligned, consecutive 40 μm sections from a P43 animal in which one eye was injected with WGA-HRP.Top, Nissl stain. Area 17 is recognizable cytoarchitectonically by the presence of small and closely packed cells in layer IV, more evident in the monocular (m) than in the binocular region, enclosed by the two gray arrows (b). The transneuronal WGA-HRP labeling (bottom) is found mainly in area 17. Note the densest geniculocortical projection in the monocular region. Very pale transneuronal labeling is also present laterally to area 17 (up to thewhite arrow, area 18a).
Fig. 4.
Fig. 4.
Flattened surfaces of the posterior portion of the two hemispheres demonstrating the extent of the primary visual area as shown by the transneuronal labeling of geniculocortical terminals (dark areas) after an intraocular injection of WGA-HRP. On the side contralateral to the injected eye, the labeling is very intense, covering both the monocular and binocular regions of the visual cortex. On the side ipsilateral to the injected eye, the labeling is more restricted; its intensity and boundaries varied from animal to animal. This area of labeling defines the binocular zone. The figures are negatives of dark-field photomicrographs of a single section each.
Fig. 5.
Fig. 5.
Tangential sections through the flattened surface of the hemispheres demonstrating transneuronal labeling of geniculocortical terminals after an injection of WGA-HRP into nondeprived eye (ltd3, ltd2, ltd6, ltd7) or deprived eye (ltd4, ltd8, ltd5, ltd1). All animals were deprived for 40 d, ending at P60. Note in the hemisphere ipsilateral to the injected eye the strong transneuronal labeling when the nondeprived pathway was labeled and the reduced labeling when the deprived eye was injected. In contrast, a clear effect of MD on the projections serving the contralateral eye was observed only inltd1, in which the deprived eye was injected with WGA-HRP. In this case, the lateral third of the visual cortex, presumably corresponding to the binocular zone, was less strongly labeled.
Fig. 6.
Fig. 6.
A, Series of anteroposterior coronal sections through the LGN contralateral and ipsilateral to a monocular injection of fluorescent dextran. The portion of the LGN receiving ipsilateral retinal fibers is confined to a small patch in the rostral half of the LGN. Dorsal is up and to theright in ipsilateral sections; up and to the left in contralateral sections. B, Example of a biocytin injection and its relation to the ipsilateral retinal projections. Left panel, Scan of fluorescent photomicrograph of an LGN coronal section showing the rhodamine dextran-labeled terminals arising from the ipsilateral eye.Right panel, Scan of a confocal image of the same section after biocytin histochemistry showing the biocytin injection site. The rhodamine-labeled area from the fluorescent photomicrograph has been superimposed to show that the injection site, located next to the pia in the dorsolateral portion of the LGN, did not overlap with the “ipsilateral patch.”
Fig. 7.
Fig. 7.
A, Scan of a photomicrograph of a coronal section through the visual cortex showing dense cortical labeling of biocytin-filled geniculocortical afferents. Note the abundant innervation not only of layer IV but also of the supragranular layers. B, C, Branches of biocytin-labeled geniculocortical arbors presented as a collage of photomicrographs combining serial focal planes. Note inB the ramifications running beneath the pial surface. Note in C branches running in layer IV. Scale bars:A, 200 μm; B, 50 μm;C, 20 μm.
Fig. 8.
Fig. 8.
Computer reconstructions of geniculocortical arbors in area 17 comparing normal P40 (A) and P60 (B) mice. The arrowheadsindicate the boundary of layer IV. All arbors are presented in coronal view, and the most complex arbors are also presented in surface view after a 90° rotation along an axis passing through layer IV (mo2a, mo2g, mo4b, mo4c, insets). Theline above coronal views indicates the pial surface. The scale is for all arbors.
Fig. 9.
Fig. 9.
Single, serially reconstructed geniculocortical arbors in area 17 in P40 animals monocularly deprived for 20 d starting at P20. A, Arbors serving the deprived eye.B, Arbors serving the nondeprived eye. Thearrowheads indicate the boundary of layer IV. The scale is for both groups of arbors.
Fig. 10.
Fig. 10.
Single, serially reconstructed geniculocortical arbors in area 17 in P60 animals monocularly deprived for 40 d starting at P20. A, Arbors serving the deprived eye.B, Arbors serving the nondeprived eye. Thearrowheads indicate the boundary of layer IV. The scale is for both groups of arbors.
Fig. 11.
Fig. 11.
Scattergrams of the total length (A) and number of branch points (B) for arbors reconstructed in normal animals (N) and for both deprived (D) and nondeprived (ND) arbors reconstructed in MD animals. The age at perfusion is also indicated (P40 and P60). The white bar represents the mean value in each group. C, Values of total length (filled bars) and number of branch points (open bars) of arbors in the six experimental groups normalized relative to the mean values of arbors in normal arbors at P40.
Fig. 12.
Fig. 12.
Intrinsic signal optical responses in mouse visual cortex. A–D, Normal mouse. E–H, Hemisphere ipsilateral to deprived eye in MD mouse.I–L, Hemisphere contralateral to deprived eye in MD mouse. Darkness indicates response to visual stimulation as percent change in reflectance as on the scale to theleft of each row. A, E, I, Responses elicited from eye contralateral (contra) to the hemisphere imaged. B, F, J, Responses elicited from eye ipsilateral (ipsi) to the hemisphere imaged on scales identical to A, E, and I.C, G, K, Ratio between activation by contralateral and ipsilateral eyes, with darkness indicating greater response to contralateral and lightness indicating greater response to ipsilateral eye. D, H, L, Images of blood vessels on the cortical surface aligned with optical maps in the same row. Monocular and binocular zones of cortex are outlined in a normal case (D), along with electrode penetration sites. Receptive fields of neurons recorded at the leftmost site were in the monocular segment of the visual field; receptive fields at two sites to the right were located successively more central and in the binocular visual field. Note the virtual disappearance of the deprived eye responses in the ipsilateral hemisphere (F) and the increase in the response to the nondeprived eye in its ipsilateral hemisphere (J). Note also the reduction in the deprived eye’s response in its contralateral hemisphere (I). Length scale, 1 mm for all images. Rostral is up and caudal is down in all figures. Medial is left in A–D andI–M, whereas medial is right inE–H. Lateral is right inA–D and I–M, whereas lateral isleft in E–H.
Fig. 13.
Fig. 13.
CBI (mean and individual values) and ocular dominance in normal and monocularly deprived animals after different deprivation protocols. A, Single neuron responses in normal mice are dominated by the contralateral eye (mean CBI = 0.75). After monocular deprivation, CBIs in the visual cortex ipsilateral to the open eye decrease to 0.45 and 0.39 after 20 and 40 d of MD, respectively, indicating dominance of the ipsilateral eye. Late MD, from P40 to 60, is still able to affect the eye dominance of visual cortical neurons. B–E, Percent of cells assigned to each of the seven ocular dominance classes (Hubel and Wiesel, 1962) in normal animals and in animals monocularly deprived from P20 to P40, from P20 to P60, and from P40 to P60, respectively. The number on top of each ocular dominance class indicates the actual number of cells.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Antonini A, Stryker MP. Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion the cat. J Comp Neurol. 1996;369:64–82. - PubMed
    1. Antonini A, Stryker MP. Effect of sensory disuse on geniculate afferents to cat visual cortex. Vis Neurosci. 1998;15:401–409. - PMC - PubMed
    1. Antonini A, Gillespie DC, Crair MC, Stryker MP. Morphology of single geniculocortical afferents and functional recovery of the visual cortex after reverse monocular deprivation in the kitten. J Neurosci. 1998;18:9896–9909. - PMC - PubMed
    1. Blakemore C, Vital-Durand F, Garey LJ. Recovery from monocular deprivation in the monkey. I. Reversal of physiological effects in the visual cortex. Proc R Soc Lond B Biol Sci. 1981;213:399–423. - PubMed
    1. Bonhoeffer T, Grinvald A. Optical imaging of the functional architecture in cat visual cortex: the layout of direction and orientation domains. Adv Exp Med Biol. 1993;333:57–69. - PubMed

Publication types

LinkOut - more resources