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T A Woolsey

Publications and source records attributed to T A Woolsey.

86 records · Page 5Linked to original sources
PubMed1970

The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units.

This article traces the author's personal history in neuroanatomical studies of the cerebral cortex including his father's pioneering studies using electrophysiology and early neuroanatomical methods. By providing the background context for the observations reported in the original heavily cited Brain Research article, the author describes how his methods of investigation with celloidin embedded material prepared with the Golgi method and Nissl staining revealed for the first time the “barrel fields” of the mouse cerebral cortex that are activated by stimulation of the facial vibrissae (whiskers). The original article reviewed the series of studies published on the murine cortical field in what later was termed a Brain Research Review. Those original observations opened an entire field of cortical organization and function that has remained an active and fertile field of neuroscience investigation.

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Blood flow dynamics in different layers of the somatosensory region of the cerebral cortex on the rat during mechanical stimulation of the vibrissae.

The present work reports studies of the quantitative spatial and temporal characteristics of changes in local blood flow in different layers of the somatosensory cortex of rats during adequate mechanical stimulation of the vibrissae. Studies were performed using 34 Wistar rats. Skull trepanning was performed under urethane (1 g/kg) anesthesia. Television-guided microscopy was used to introduce a set of three platinum electrodes (100 microns in diameter, with tip diameters of 30-40 microns) into the somatosensory cortex projection zone of the vibrissae. The first and third electrodes were positioned in cortical layers I-III and IV-VI and the central electrode was used to generate hydrogen within the tissue. Electrode positions were confirmed histologically after experiments. Animals were placed on artificial ventilation and one or all vibrissae were stimulated at a frequency of 3 Hz for 60 sec, with interstimulus intervals of 3 min. Changes in the local blood flow were measured during stimulation and for 1 min afterwards, using the hydrogen clearance method, and brain tissue impedance was also measured. There was a small (up to 5-7%) reduction in blood flow in the first seconds of stimulation, which was followed 15-25 sec later by an increase and subsequent return to initial when stimulation stopped. The increases in blood flow during stimulation of all vibrissae were by 24.2 +/- 6.7% (n = 36) in layers IV-VI and 24.5 +/- 5.6% (n = 34) in layers I-III; increases in response to stimulation of single vibrissae were by 19.4 +/- 7.4% (n = 28) and 17.8 +/- 6.4% (n = 28) respectively. The dynamics of impedance changes corresponded to those of blood flow changes. Thus, heterogeneity was found in changes of local brain blood flow in different layers of the somatosensory cortex during increases in cortical functional activity.

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Growth of thalamic afferents into mouse barrel cortex.

We studied thalamocortical afferent (TCA) growth into somatosensory cortex as the whisker barrels emerge in postnatal mice. Ingrowing fibers from the ventrobasal (VB) thalamus were selectively labeled by two means. Under direct vision, individual axons and populations of axons were labeled in vitro with HRP, or in fixed tissue with Dil (1,1'-dioctodecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate), in pieces of brain containing both the source nucleus in the thalamus and its cortical target. Many simple thalamocortical afferents are already within the upper cortical plate at birth [postnatal day one (PND1)]. Initially, TCAs from each point in the thalamus distribute in the cortex as two-dimensional "Gaussians," which overlap laterally to constitute a uniform projection pattern. The projection is topographic, because adjacent focal injections within VB label adjacent cortical loci. Subsequent development of barreloids (thalamic representations of the whiskers) partitions the TCA projection into a set of whisker-related Gaussians, centered on cortical targets whose collective topography reflects that of the source pattern. After barreloids form on about PND3, but before barrels appear in cytoarchitecture on about PND5, the overlapping TCAs segregate into dense terminal clusters in layer IV, around which barrels later mature. Time series of single fibers traced with camera lucida explain this transformation that is so noticeable at the population level. As early as PND1, individual TCAs emit multiple ascending collaterals on their horizontal run through white matter and oblique ascent into upper cortex. Subsequently, by PND4, and proceeding at least through PND7, there is accelerated terminal arborization of selected appropriate collateral branches and pruning back of other inappropriate ones. The selection mechanism appears to result from within-group reinforcement events that are stronger for branches toward the center of each whisker-related Gaussian distribution.

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Computer-aided analyses of thalamocortical afferent ingrowth.

Segregation of thalamocortical afferent (TCA) fibers precedes barrel formation in rodent somatosensory cortex (Killackey and Leshin, 1975; Jeanmonod et al., 1981; Jensen and Killackey, 1987b; Senft, 1989; Erzurumlu and Jhaveri, 1990). Hypotheses about the arborization strategies followed by these ingrowing fibers have been generated from evaluation of labeled terminal fragments of mouse TCAs (Senft and Woolsey, 1991a). Those TCAs were of necessity truncated by the histological processing needed to observe them at high resolution. This fragmentation, along with biological variability, forces conclusions about single intact axons to be derived from populations of parts of arbors. To evaluate the hypotheses critically, we designed a computer program to quantify morphological aspects of labeled TCAs drawn with a camera lucida. We constructed algorithms to abstract, from fiber populations, properties minimally affected by truncation. Our program analyzes, and displays as histograms, fiber and branch densities and orientations. To represent these features by additional graphical means, "average" ingrowing TCAs were generated, based on the accumulated statistics of the traced fiber fragments. Quantitative descriptions of TCA populations from postnatal day 1 (PND1) through PND7 are presented. These analyses show that fibers and their branches accumulate with age within the cortical plate (emergent layer IV), and to a lesser extent within developing layer VI. Simultaneously, the distributions of these afferents within cortical laminae transform from uniform to patchy in the plane of the cortex. Peaks exhibit the periodicity typical of mature barrels. Branches become more numerous focally as and where layer IV barrels emerge. Individually traced arbors show reduced total widths consistent with progressive pruning of branches extending into territories of inappropriate barrels, both in layer IV and deeper in the cortex.

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Mouse barrel cortex viewed as Dirichlet domains.

Barrels are patterned groups of neurons in rodent somatosensory cortex that correspond one to one with the animal's facial whiskers. Dirichlet domains are a class of convex polygon found frequently in nature, often arising by nucleation from center points. Analytic and graphical methods were devised to verify the hypothesis that Dirichlet domains accurately describe the adult barrel fields of normal mice. We found that normal barrel fields and abnormal barrel fields caused by supernumerary whiskers or lesions to the whisker pad are closely approximated by this mathematical formalism. This implies that each developing cortical barrel organizes about a center point. Experiments in neonatal animals (Senft and Woolsey, 1991a) demonstrate foci in the thalamocortical afferent (TCA) distributions. These results support an hypothesis in which TCAs are the nucleating agents causing barrels to organize as Dirichlet domains. This is made possible because TCA terminals from each barreloid (a whisker-related group of cells in the ventrobasal complex of the thalamus) initially colonize somatosensory cortex with an approximately "Gaussian" distribution. These peaked groups of related TCAs behave as Dirichlet domain centers. They generate barrel structures competitively, in animals with normal or with perturbed whisker patterns, via statistical epigenetic interactions within and between distinct TCA Gaussians associated with separate whiskers. This leads to selective axon outgrowth and pruning of single TCA branches, regulated by the TCA population, and creates beneath each Gaussian the dense knot of related TCA arbors typical of the barrel cortex. Similar parcellation of neuronal processes into contending subgroups having spatially coherent actions could lead to nucleation of other geometric patterns as Dirichlet domains elsewhere in the brain.

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Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain.

How neuronal activity changes cerebral blood flow is of biological and practical importance. The rodent whisker-barrel system has special merits as a model for studies of changes in local cerebral blood flow (LCBF). Stimulus-evoked changes in neural firing and 'intrinsic signals' recorded through a cranial window were used to define regions of interest for repeated flow measurements. Whisker-activated changes in flow were measured with intravascular markers at the pia. LCBF changes were always prompt and localized over the appropriate barrel. Stimulus-related changes in parenchymal flow monitored continuously with H2 electrodes recorded short latency flow changes initiated in middle cortical layers. Activation that increased flow to particular barrels often led to reduced flow to adjacent cortex. Dye was injected into single penetrating arterioles from the pia of the fixed brain and injected into arterioles in slices of cortex where barrels were evident without stains. Arteriolar and venular domains at the surface were not directly related to underlying barrels. Capillary tufts in layer IV were mainly coincident with barrels. The matching between a capillary plexus (a vascular module) and a barrel (a functional neuronal unit) is a spatial organization of neurons and blood vessels that optimizes local interactions between the two. The paths of communication probably include: neurons to neurons, neurons to glia, neurons to vessels, glia to vessels, vessels to vessels and vessels to brain. Matching a functional grouping of neurons with a vascular module is an elegant means of reducing the risk of embarrassment for energy-expensive neuronal activity (ion pumping) while minimizing energy spent for delivery of the energy (cardiac output). For imaging studies this organization sets biological limits to spatial, temporal and magnitude resolution. Reduced flow to nearby inactive cortex enhances local differences.

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[Cerebral blood flow and cerebrovascular reactivity in the early postnatal ontogeny of rats].

The development of cortical cerebral blood flow (CBF) and cerebrovascular reactivity (CVR) were studied in Wistar rats during early postnatal ontogenesis, in groups aged 2-5, 6-8, 9-11, 12-15, 16-18 and 19-25 days. CBF was measured polarographically using inhaled hydrogen clearance method, with platinum electrodes inserted into parietal cortex. At the mentioned age periods, CBF and its percentage of adult level averaged as 38 (21%), 81 (45%), 142 (78%), 85 (47%), 110 (61%), and 118 (65%) ml/100 g/min, respectively. Hence, during the early postnatal ontogenesis CBF increased gradually, however, it did not reach the adult level up to the end of the first month. CBF peak at 9-11 days period is suggested as a result of sharp rise of the brain vessels growth. CVR was assessed as the percentage of CBF increase after standardized 5% CO2 inhalation test. At the above age periods, CVR was found to bi 26, 33, 36, 41, 44 and 31% respectively, and was similar to adult rat CVR of 36%. The conclusion was drawn that regulatory mechanisms of adequate responses of brain vasculature to chemical metabolic factors are well developed already at the very beginning of postnatal life.

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