DOI: 10.1126/science.287.5460.2029. Rapid Extragranular Plasticity in the Absence of Thalamocortical Plasticity in the Developing Primary Visual Cortex

Rapid Extragranular Plasticity in the Absence of Thalamocortical Plasticity in the Developing Primary Visual Cortex

10.1126/science.287.5460.2029

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Monocular deprivation during early postnatal development remodels the circuitry of the primary visual cortex so that most neurons respond poorly to stimuli presented to the deprived eye. This rapid physiological change is ultimately accompanied by a matching anatomical loss of input from the deprived eye. This remodeling is thought to be initiated at the thalamocortical synapse. Ocular dominance plasticity after brief (24 hours) monocular deprivation was analyzed by intrinsic signal optical imaging and by targeted extracellular unit recordings. Deprived-eye responsiveness was lost in the extragranular layers, whereas normal binocularity in layer IV was preserved. This finding supports the hypothesis that thalamocortical organization is guided by earlier changes at higher stages.

Bibliography

Trachtenberg, J. T., Trepel, C., & Stryker, M. P. (2000). Rapid Extragranular Plasticity in the Absence of Thalamocortical Plasticity in the Developing Primary Visual Cortex. Science, 287(5460), 2029â2032.

Authors 3

Joshua T. Trachtenberg (first)
Christopher Trepel (additional)
Michael P. Stryker (additional)

References 32 Referenced 201

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Shatz C. J., Stryker M. P., J. Physiol. 281, 267 (1978). (10.1113/jphysiol.1978.sp012421) / J. Physiol. by Shatz C. J. (1978)
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10.1126/science.279.5350.566
10.1016/S0896-6273(00)80941-1
All deprivations and recordings were carried out between postnatal days 27 and 33.
Values for individual pixels in the OD maps were computed from each pixel of the unfiltered blank-normalized images by comparing the response strengths to stimulation of the two eyes at the orientation producing the greatest response. This procedure is similar to that used to determine OD in single-unit recordings where the responses to optimal stimuli in the two eyes are compared. It is different from the conventional OD ratio maps which compare the average rather than the optimal responses.
10.1113/jphysiol.1962.sp006837
Comparison of single-unit and optical imaging data in the deprived animals demonstrates that the optical signals reflected a large contribution from activity in layer IV. This is consistent with the reduced thickness of the upper layers at the crown of the gyrus and the scant myelination of the cortex at this age leading to little light scatter as well as with the narrow depth of field of the tandem lens optical system focused within layer IV at a depth of 400 μm leading to a more than sixfold reduction in the contrast of structures the size of OD columns in the upper 100 μm of cortex. D. Malonek et al. (22) report a 25% contribution from a depth of 800 μm in monkey cortex with similar imaging optics; the layer IV contribution to the optical signal in our experiments would be expected to be at least two times as great.
The OD of single units was assessed on the conventional 1-to-7 scale of (10). Classification of OD was done blind; that is one experimenter who was unable to observe the animal because of an interposed screen classified cells as binocular (OD = 4) one category off center in favor of the first or second eye (OD = 3 or 5) two off center (OD = 2 or 6) or an extreme (OD = 1 or 7). Manipulation of the individual eye shutters was performed by the second experimenter who also recorded the OD rating provided by the first experimenter.
χ 2 values were calculated from raw data. As we compressed the standard seven-bin histograms into five bins the χ 2 ( n − 1) statistic had four degrees of freedom. This adjustment was made because we recorded neither cells in extreme OD categories during control experiments nor closed-eye dominant cells from experimental animals.
Whereas OD ranking classifies the ratio of contralateral to ipsilateral eye input to a single unit the ODI measures the degree to which the entire population of units is dominated by the nondeprived eye (or right eye in controls). For cells recorded in the hemisphere ipsilateral to the deprived eye the ODI is calculated as ODI=(N1−N7)+23(N2−N6)+13(N3−N5)+NT2NTwhereas for cells recorded in the hemisphere contralateral to the deprived eye the index equals 1 − ODI. In this equation N T is the total number of visually responsive units and N x is the number of units with OD rating x. An ODI of 0 indicates that the deprived eye dominates the population of measured units whereas an ODI of 1 indicates that the nondeprived eye dominates the population. This index is designed so that a one-category error in the assessment of OD would cause the same change in the value of the ODI no matter in which OD category it occurs. The MI reflects the degree to which cortical responses are dominated by one eye or the other but not by both. The MI is defined as MI=(N1+N7)+23(N2+N6)+13(N3+N5)NTAn MI of 0 suggests that all individual cells are driven equally by both eyes whereas an MI of 1 suggests that all cells are driven exclusively by one eye or the other. These indices are similar to those described in (23).
Olson C., Freeman R. D., J. Neurophysiol. 38, 26 (1975); (10.1152/jn.1975.38.1.26) / J. Neurophysiol. by Olson C. (1975)
Movshon J. A., Dursteler M. R., J. Neurophysiol. 40, 1255 (1977). (10.1152/jn.1977.40.6.1255) / J. Neurophysiol. by Movshon J. A. (1977)
Daw N. W., Fox K., Sato H., Czeptia D., J. Neurophysiol. 67, 197 (1992). (10.1152/jn.1992.67.1.197) / J. Neurophysiol. by Daw N. W. (1992)
10.1126/science.8091215
. This somatic sensory cortical phenomenon differs from that found here in that it lacks a critical period is not the first stage of an anatomical reorganization and represents an increase in response strength rather than a loss of response.
Mitchell D. E., Philos. Trans. R. Soc. London Ser. B Biol. Sci. 333, 51 (1991). (10.1098/rstb.1991.0060) / Philos. Trans. R. Soc. London Ser. B Biol. Sci. by Mitchell D. E. (1991)
Gilbert C. D., Wiesel T. N., Nature 280, 120 (1979). (10.1038/280120a0) / Nature by Gilbert C. D. (1979)
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D. O. Hebb The Organization of Behavior. A Neuropsychological Theory (Wiley New York 1949);
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Friedman D. F., Hess G., Donoghue J. P., Rioult-Pedotti M. S., Nature Neurosci. 1, 230 (1998); (10.1038/678) / Nature Neurosci. by Friedman D. F. (1998)
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D. Malonek D. Shoham E. Ratzlaff A. Grinvald paper presented at the 20th Annual Meeting of the Society for Neuroscience St. Louis MO 28 October 1990.
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Supported by NIH grant R37-EY02874 to M.P.S. a National Research Service Award (EY06824) to J.T.T. and Natural Sciences and Engineering Research Council of Canada and Fight for Sight (research division of Prevent Blindness America) postdoctoral fellowships to C.T.

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 5:35 a.m.)
Deposited	1 year, 7 months ago (Jan. 13, 2024, 5:45 a.m.)
Indexed	1 day, 15 hours ago (Aug. 30, 2025, 1:08 p.m.)
Issued	25 years, 5 months ago (March 17, 2000)
Published	25 years, 5 months ago (March 17, 2000)
Published Print	25 years, 5 months ago (March 17, 2000)

Funders 0

None

BibTeX

@article{Trachtenberg_2000, title={Rapid Extragranular Plasticity in the Absence of Thalamocortical Plasticity in the Developing Primary Visual Cortex}, volume={287}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.287.5460.2029}, DOI={10.1126/science.287.5460.2029}, number={5460}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Trachtenberg, Joshua T. and Trepel, Christopher and Stryker, Michael P.}, year={2000}, month=mar, pages={2029–2032} }

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