Differential metabolic and electrical activity in the somatic sensory cortex of juvenile and adult rats

We have examined relative levels of metabolic and electrical activity across layer IV in the primary somatic sensory cortex (S1) of the rat in relation to regions of differential postnatal cortical growth. Each of several indices used--mitochondrial enzyme histochemistry, microvessel density, Na+/K+ pump activity, action potential frequency, and deoxyglucose uptake--indicate regional variations of metabolic and electrical activity in this part of the brain in both juvenile (1-week- old) and adult (10–12-week-old) animals. At both ages, areas of the somatic sensory map related to special sensors such as whiskers and digital pads showed evidence of the most intense activity. Thus, mitochondrial enzyme staining, blood vessel density, and Na+/K+ ATPase activity were all greatest in the barrels and barrel-like structures within S1, and least in the adjacent interbarrel cortex and the cortex surrounding S1. Multiunit recordings in and around the posteromedial barrel subfield of anesthetized animals also showed that the average ratio of evoked to spontaneous activity was greater in barrels than in the surrounding, metabolically less active cortex. Furthermore, autoradiograms of labeled deoxyglucose accumulation in awake behaving animals indicated systematic differences in neural activity across S1 barrels and barrel-like structures showed more deoxyglucose accumulation than interbarrel, nonbarrel, or peri-S1 cortex. These regional differences in neural activity correspond to regional differences in neocortical growth (Riddle et al., 1992). The correlation of greater electrical activity, increased metabolism, and enhanced cortical growth during postnatal maturation suggests that neural activity foments the elaboration of circuitry in the developing brain.

[1]  J. Rushen Neural activity and the growth of the brain , 1995 .

[2]  Dale Purves,et al.  Neural Activity And The Growth Of The Brain , 1994 .

[3]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[4]  D. Purves,et al.  Iterated patterns of brain circuitry (or how the cortex gets its spots) , 1992, Trends in Neurosciences.

[5]  D. Purves,et al.  Growth of the rat somatic sensory cortex and its constituent parts during postnatal development , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R. Rhoades,et al.  Postnatal blockade of cortical activity by tetrodotoxin does not disrupt the formation of vibrissa-related patterns in the rat's somatosensory cortex. , 1992, Brain research. Developmental brain research.

[7]  R. Hevner,et al.  Coordination of ATP production and consumption in brain: Parallel regulation of cytochrome oxidase and Na+, K+-ATPase , 1992, Neuroscience Letters.

[8]  M F Jacquin,et al.  Infraorbital nerve blockade from birth does not disrupt central trigeminal pattern formation in the rat. , 1992, Brain research. Developmental brain research.

[9]  D Purves,et al.  Specialized vascularization of the primate visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  D. O'Leary,et al.  Potential of visual cortex to develop an array of functional units unique to somatosensory cortex , 1991, Science.

[11]  C. Shatz Impulse activity and the patterning of connections during cns development , 1990, Neuron.

[12]  R. C. Collins,et al.  Metabolic anatomy of brain: A comparison of regional capillary density, glucose metabolism, and enzyme activities , 1989, The Journal of comparative neurology.

[13]  R. Northcutt Body and Brain. A Trophic Theory of Neural Connections. Dale Purves. Harvard University Press, Cambridge, MA, 1988. viii, 231 pp., illus. $35. , 1989, Science.

[14]  M. Wong-Riley Cytochrome oxidase: an endogenous metabolic marker for neuronal activity , 1989, Trends in Neurosciences.

[15]  I. Silver,et al.  ATP and Brain Function , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[16]  D. Purves Body and Brain: A Trophic Theory of Neural Connections , 1988 .

[17]  M. N. Wallace Histochemical demonstration of sensory maps in the rat and mouse cerebral cortex , 1987, Brain Research.

[18]  H. Killackey,et al.  The organization and mutability of the forepaw and hindpaw representations in the somatosensory cortex of the neonatal rat , 1987, The Journal of comparative neurology.

[19]  Jeff W. Lichtman,et al.  Principles of neural development , 1985 .

[20]  U. Patel-Vaidya,et al.  Ultrastructural organization of posterior and anterior barrels in the somatosensory cortex of rat , 1985, Journal of neuroscience research.

[21]  J. Chapin,et al.  Mapping the body representation in the SI cortex of anesthetized and awake rats , 1984, The Journal of comparative neurology.

[22]  L. Sokoloff Metabolic probes of central nervous system activity in experimental animals and man , 1984 .

[23]  Urmi Patel,et al.  Non-random distribution of blood vessels in the posterior region of the rat somatosensory cortex , 1983, Brain Research.

[24]  L. Sokoloff,et al.  Localization of Functional Activity in the Central Nervous System by Measurement of Glucose Utilization with Radioactive Deoxyglucose , 1981, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[25]  Louis Sokoloff,et al.  Activity‐dependent Energy Metabolism in Rat Posterior Pituitary Primarily Reflects Sodium Pump Activity , 1980, Journal of neurochemistry.

[26]  L. Sokoloff,et al.  Mapping of local cerebral functional activity by measurement of local cerebral glucose utilization with [14C]deoxyglucose. , 1979, Brain : a journal of neurology.

[27]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[28]  D. Simons,et al.  Functional organization in mouse barrel cortex , 1979, Brain Research.

[29]  H. Killackey,et al.  The formation of afferent patterns in the somatosensory cortex of the neonatal rat , 1979, The Journal of comparative neurology.

[30]  D. Simons Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[31]  L. Sokoloff,et al.  RELATION BETWEEN PHYSIOLOGICAL FUNCTION AND ENERGY METABOLISM IN THE CENTRAL NERVOUS SYSTEM , 1977, Journal of neurochemistry.

[32]  F. Sharp Relative cerebral glucose uptake of neuronal perikarya and neuropil determined with 2-deoxyglucose in resting and swimming rat , 1976, Brain Research.

[33]  W. L. Stahl,et al.  Histochemical localization of potassium-stimulated P-nitrophenylphosphatase activity in the somatosensory cortex of the rat. , 1976, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[34]  Stahl Lw,et al.  Localization of Na+, K+-ATPase in brain. , 1976 .

[35]  C. Welker Receptive fields of barrels in the somatosensory neocortex of the rat , 1976, The Journal of comparative neurology.

[36]  H. Killackey,et al.  Anomalous organization of thalamocortical projections consequent to vibrissae removal in the newborn rat and mouse , 1976, Brain Research.

[37]  S. H. Broderson,et al.  Localization of Na+, K+-ATPase in brain. , 1976, Federation proceedings.

[38]  D. F. Wann,et al.  Mouse SmI cortex: qualitative and quantitative classification of golgi-impregnated barrel neurons. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[39]  T. Woolsey,et al.  Structure of layer IV in the somatosensory neocortex of the rat: Description and comparison with the mouse , 1974, The Journal of comparative neurology.

[40]  T. Woolsey,et al.  The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex , 1970 .

[41]  H. Hess,et al.  INTRALAMINAR DISTRIBUTION OF Na+‐K+ ADENOSINE TRIPHOSPHATASE IN RAT CORTEX , 1964, Journal of neurochemistry.

[42]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[43]  A. Campbell VARIATION IN VASCULARITY AND OXIDASE CONTENT IN DIFFERENT REGIONS OF THE BRAIN OF THE CAT , 1939 .