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The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex

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The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex The Journal of Neuroscience, October 15, 2000, 20(20):7579–7586 The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex Carl C. H. Petersen and Bert Sakmann Department of Cell Physiology, Max-Planck-Institute for Medical Research, Heidelberg D-69120, Germany Sensory whiskers are mapped to rodent layer 4 somatosensory were found to attenuate at barrel borders. This ensemble prop- cortex as discrete units termed barrels, which can be visualized erty of a layer 4 barrel was further investigated by analyzing the at high resolution in living brain slices. Both anatomical and connectivity of pairs of excitatory neurons with respect to the physiological properties of the layer 4 neuronal network can thus locations of the somata. Approximately one-third of the excita- be investigated in the context of the functional boundaries of this tory neurons within the same barrel were synaptically coupled. At sensory map. Large-scale confinement of neuronal arbors to the septum between adjacent barrels the connectivity dropped single barrels was suggested by restricted lateral diffusion of DiI rapidly, and very few connections were found between neurons across septa between barrels. Morphological analysis of den- located in adjacent barrels. Each layer 4 barrel is thus composed dritic and axonal arborizations of individual excitatory neurons of an excitatory neuronal network, which to a first order approx- showed that neuronal processes remain within the barrel of origin imation, acts independently of its neighbors. through polarization toward the center of the barrel. Functionally, Key words: neocortex; somatosensory cortex; barrel cortex; the large-scale properties of the neuronal network were investi- layer 4; synaptic transmission; EPSP; glutamate; neuronal net- gated through mapping the spatial extent of field EPSPs, which work; dendritic morphology; axonal morphology Sensory input is mapped to the neocortex such that closely related The functional data are reflected also in the underlying anatomy of sensory stimuli are also close to each other spatially in the cortical the axonal and dendritic arbors, which are largely confined to representation. How individual neurons and neuronal circuits are individual barrels. Neighboring barrels thus appear to be only functionally arranged within these maps is not well understood. weakly connected to each other, and as a first order approximation This is in large part attributable to the difficulties of simultaneously we may consider each barrel as an isolated neuronal network. Such studying both synaptic transmission between individual identified functionally independent neuronal networks of defined numbers of neurons and locating the neurons within the sensory map. The neurons and defined connectivity offer an opportunity to study the barrel field of the rodent somatosensory cortex provides a unique activity of physiologically relevant neuronal circuits in quantitative neocortical region for such investigations. Each sensory whisker is detail. As well as providing data on how sensory information is represented somatotopically in the large-scale anatomical structure processed in the input layer of the neocortex, such a description of of a barrel in layer 4 of the neocortex (Woolsey and Van der Loos, the functional architecture is also a prerequisite for understanding 1970). These anatomically defined structures have also been inves- how reorganization of cortical representation occurs at a cellular tigated electrophysiologically by extracellular unit recordings, and level, for example after deprivation of sensory input (Diamond et the location of the recording electrode within the barrel field is al., 1994; Glazewski and Fox, 1996; Finnerty et al., 1999; Polley et found to be homologous to the physiologically defined principal al., 1999). whisker (Welker, 1976; Simons, 1978; Armstrong-James and Fox, 1987). Thus, it is possible to relate the barrel pattern of the MATERIALS AND METHODS neocortex directly to the somatosensory map. Furthermore, barrel- Slice preparation. Thalamocortical slices of 250–300 ␮m thickness were like structures are visible in the living brain slice preparation of prepared from anesthetized Wistar rats (13- to 15-d-old) following the description of Agmon and Connors (1991) with modifications by Feld- somatosensory cortex (Agmon and Connors, 1991). The neuronal meyer et al. (1999). Slices were cut by a vibratome in ice-cold extracellular circuitry can thus be investigated at the level of individual neurons medium and were subsequently incubated at 35°C for 15–30 min after and their synaptic connections in the context of the functional slicing. The slices were then transferred to room temperature (20–23°C) boundaries of this sensory map. until required for analysis. Throughout the procedure slices were main- tained in extracellular medium containing (in mM): 125 NaCl, 25 The analysis of the excitatory neuronal network of layer 4 rat NaHCO , 25 glucose, 2.5 KCl, 1.25 NaH PO ,2CaCl, and 1 MgCl barrel cortex investigated in this study is thus a step to further our 3 2 4 2 2 bubbled with 95% O2 and 5% CO2. understanding of how the first layer of the neocortical circuitry may Identification of barrels in living slices. The barrel subfield of somatosen- respond to input. In a recent study, Feldmeyer et al. (1999) de- sory cortex is easily recognized in the thalamocortical slice preparation even by the naked eye. Under low-power light microscopy (Zeiss Axioskop scribed highly reliable local synaptic connections with large NMDA fitted with a 2.5ϫ lens) the dark band of layer 4 separates into barrels receptor components between excitatory neurons of layer 4 barrel separated by lighter septal regions. To identify barrels at higher magnifi- cortex. In this study, we combine the investigation of the ensemble cations (Zeiss water-immersion lenses, 10ϫ and 40ϫ), it is essential to properties of barrels with the anatomy and physiology of individual increase contrast by closing the aperture. In this study only barrels that could be clearly distinguished at 40ϫ with high-contrast apertures and neurons and pairs of neurons with the aim of understanding the further enhanced with a camera image processor (C2400; Hamamatsu, collective properties of the underlying neuronal network. Whereas Tokyo, Japan) were used for further study. This selects for the most clearly neurons lying inside the same barrel are often synaptically con- delineated barrels and allows the detailed study of neurons in well defined nected, neurons from neighboring barrels show low connectivity. regions of a single barrel. The barrels selected by these criteria did not necessarily lie in the posterior medial barrel subfield, and thus barrels with a wide range of diameters were investigated. Received May 8, 2000; revised July 17, 2000; accepted July 25, 2000. Identification of barrels by cytochrome C stain. Fixed slices were washed C.C.H.P. was supported by a Marie Curie fellowship from the European Commis- five times with PBS (100 mM sodium phosphate, pH 7.2) over a period of sion. We thank Michael Brecht, Veronica Egger, and Dirk Feldmeyer for helpful 2 hr. Subsequently they were incubated at 35°C until clear staining of discussions and comments on this manuscript. barrels were observed (0.5–5 hr) in PBS containing (in mg/ml): 0.3 cyto- Correspondence should be addressed to Carl C. H. Petersen, Department of Cell chrome C, 0.3 catalase, and 0.5 diaminobenzidine. Slices were subsequently Physiology, Max-Planck-Institute for Medical Research, Jahnstrasse 29, Heidelberg washed five times with PBS over a period of 2 hr. D-69120, Germany. E-mail: [email protected]. Quantification of barrel boundaries. Digital photographs of barrels in Copyright © 2000 Society for Neuroscience 0270-6474/00/207579-08$15.00/0 living or stained slices were taken using either a monochromatic camera 7580 J. Neurosci., October 15, 2000, 20(20):7579–7586 Petersen and Sakmann • Excitatory Network of Layer 4 Barrel Cortex (C2400; Hamamatsu) or a color CCD camera (Seescan LC100; INTAS, potentials by injection of 5 msec duration current pulses with a threshold Go¨ttingen, Germany). The photographs were converted into grayscale of ϳ5 nA. The evoked action potentials are recorded as short duration images and imported into IgorPro (Wavemetrics, Lake Oswego, OR) for depolarizations with amplitudes of ϳ10 mV. Because of the requirements quantitative analysis. Pixel intensities were measured as a function of of strong current injections, only the Axoclamp 2A amplifier was used for position within layer 4. Maxima (bright) in this intensity function identify this recording configuration. The loose-patch configuration does not allow septal regions, which separate the low-intensity (dark) barrels. The inten- the analysis of the action potential firing pattern, giving rise to some sity function was normalized such that the lowest brightness was repre- uncertainty concerning the neurotransmitter identity of a presynaptic sented by a value of zero and the maximal brightness by one. For quanti- neuron, although this can often be judged from the appearance of the cell fication of the barrel boundary sigmoidal functions of the form (a ϩ b/ under IR-DIC. Thus, to isolate EPSPs, 10 ␮M bicuculline was included in (1 ϩ exp(cxϩ d))) were fitted, and the half-maximal brightness was chosen the extracellular medium. To test whether the loose-patch technique to indicate the edge of a barrel. provides equivalent results to whole-cell recordings, we compared EPSPs DiI injections. Barrels in
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