Brain Research, 177 (1979) 61-82 ~(')Elsevier/North-Holland Biomedical Press

61

C O N D U C T I V I T Y IN T H E SOMATOSENSORY CORTEX OF THE CAT - EVIDENCE FOR CORTICAL ANISOTROPY

PERRY B. HOELTZELL and ROBERT W. DYKES Department of Physialogy and Biophysics, Dalhousie University, Halifax, Nova Scotia (Canada)

(Accepted December 14th, 1978)

SUMMARY Orthogonal conductivity components were determined for 3 depths in the somatosensory cortex of cats and relative vertical conductivities were determined for all depths. (2) For cortical layers II-IIl, the conductivity was nearly twice as large (1.7 times) in the anteroposterior direction as it was in the mediolateral direction, whereas in layer IV the conductivity in the mediolateral direction was about 1.4 times greater than it was in the anteroposterior direction. (3) With the exception ot' the anteroposterior direction of layers II-lll and the mediolateral direction of layer IV, the vertical conductivity of the cortex was always greater than either of the horizontal conductivities. (4) Vertical conductivities varied with cortical depth. The lowest vertical conductivity occurred in layer I. It increased in layers II-lll, dropped in layer IV, and increased again in layer VI to a value comparable to layers II-lll. (5) Adjacent determinations of conductivity indicated that over short distances (1-2 ram) the cortex was electrically homogeneous. (6) These data suggest that the cellular organization of the somatosensory cortex changes markedly and abruptly with cortical depth. Furthermore, they suggest that a significant portion of the cortical neuropile in layers II Ill and in layer IV is highly polarized. The possible anatomical basis for this polarization is discussed as are the effects of cortical anisotropy upon conductivity measurements.

INTRODUCTION To analyze the distribution of electrical phenomena in the cortex one must be knowledgeable of its intrinsic electrical properties. For example, the specific impe-

62 dance of the cortex must be known before source-sink analysis can provide useful information concerning the spatial and temporal sequence of its electrical activity 4, 23-25. Although a number of studies in cats and rabbits provide specific impedance data for whole cortexSAS.34 or for the upper layers taken together 9,29,30, none provide data for the individual layers of this tissue. Recently specific impedance measurements taking into account lamination, have been made in the cerebeUar cortex of the catZS,'3'~ and in the anuran cerebellum 24. With the aid of such measurements workers have obtained data from source-sink analyses to support theories concerning the sequence of activation of neuronal populationslZ-14, '~4. Before equivalent experiments can be performed in cat cerebral cortex, specific impedance measurements must be obtained for individual layers of this tissue also. Although the need for such a layer by layer determination is not so obvious here because the cell bodies appear more randomly distributed than in the cerebellum, it does become apparent from histological considerations. From Ramon-Moliner's(26-2s) studies of the patterns of fiber and cell distributions in the somatosensory cortex of the cat, it is apparent that 85 ~,, of the volume of the cortex is occupied by nerve cell processes and extracellular space. Thus any study of the impedance of this area of cortex, as with the cerebellar cortex, is mainly a study of the resistive and capacitative effects of those cell processes, glia, vasculature and extracellular space. The quantitative data of Ramon-Moliner show clear differences in the densities of fibers as a function of cortical depth as well as differences in dendritic densities and dendritic lengths. From these data it can be inferred that conductivity is likely to change with depth. To test this hypothesis, the vertical conductivity of somatosensory cerebral cortex was determined on a layer by layer basis. In addition, there is circumstantial evidence that horizontal anisotropy* may occur; in the cortex, there are reports of several cell types having dendritic distributions elongated in a direction parallel to the cortical surface. In monkeys, Jones TM described 9 types of non-pyramidal cells, each with a characteristic dendritic and axonal organization and optimum depth of distribution. Five had primarily verticallyoriented fiber (axonal and dendritic) distributions, but two others had preferred orientations in the horizontal plane, both in the anteroposterior direction: (perpendicular to the central sulcus). Also, Marin-PadiUa and Stibitz is have provided computer representations of certain cells in layers II-V of human cerebral cortex which were enclosed within an elongated territory perpendicular to the precentral gyrus. If such anisotropy exists it has important implications for cortical function. Thus, experiments were devised to measure the specific impedance of the somatosensory cerebral cortex on a layer-by-layer basis in a manner capable of demonstrating the existence of cortical anisotropy.

* In this context, anisotropy implies that conductivity will be a function of direction only. This should not be confused with non-homogeneity which implies that conductivity changes as a function of distance, but implies no dependence upon direction. A medium that is anisotropic may or may not be homogeneous.

63 METHODS A N D P R O C E D U R E

Surgical preparation. The data were collected from cats of either sex, generally weighing no more than 3.2 kg. Larger cats were not used because of unacceptably large cerebrovascular pulsations and because, in these animals, difficulties were encountered with the penetration of recording electrodes through the pia mater; unacceptably large movements of the previously positioned current injection electrode were produced. After fasting for one day, each cat was anesthetized with an intraperitoneal injection of sodium pentobarbital (35 mg/kg). A venous catheter was inserted for administration of additional doses of anesthetic and an injectable cortisone (Solucotter, 10 mg/kg, Upjohn). The animal was artificially ventilated (pCO2 was maintained between 3.6 and 4.0 ~ ) and core temperature was maintained between 36 and 37 °C.

The animal's head was positioned in a modified stereotaxic instrument and a craniotomy performed. The skin edges were sutured to a ring to form a pool for saline, the dura was removed, and the cortex was immediately covered with warmed, phosphate-buffered saline (pH 7. l). Care was taken to avoid cooling or drying of the cortical surface. The cortex was never left exposed to air since transient drying of the pia-arachnoid can radically alter the surface impedancO. Meticulous attention was given to the physiological state of the cortex. Any sign of edema, vasodilation, or stasis in the capillaries was cause for termination of the experiment. The anesthetic level was kept sufficiently light so that withdrawal reflexes could be elicited by noxious stimuli. Single unit and EEG activity were observed during placement of the recording electrode. The coordinates. Conductivity components were measured along the axes of a cartesian coordinate system. If anisotropy existed it would have been most apparent if its major axis was aligned with one of the axes of the coordinate system used for data collection. There is no data for the cat which might suggest how such an axis of polarization might be aligned, however, the work of Jones 10 and Marin-Padilla iv, showed that in monkeys and man some neuronal elements were elongated in an anteroposterior direction perpendicular to the central sulcus, suggesting that such cells might be present in the cat. Since in the cat, the post-cruciate dimple (pcd) is considered to be the analog of the central sulcus it was used as the orienting landmark (Fig. 1). Cytoarchitectonic maps of this area 7 show that areas 4, 3, 1 and 2 run parallel to the pcd until these fields are about 4 mm away from the pcd in the posterior and 2 mm away in the lateral direction. Thus, the coordinate system was aligned so that the y-axis was parallel to the presumed direction ofthecytoarchitectonic fields and the xaxis was perpendicular to the analog of the central sulcus. The z-axis was perpendicular to the cortical surface. The somatosensory cortex was divided into 6 layers '~v. Due to the thinness of layer |! it was not possible to distinguish its conductivity from that of layer Ill. Consequently the two were treated as one region. Also because it was so narrow, no conductivity data were obtained for layer V.

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Conductivity in the somatosensory cortex of the cat -- evidence for cortical anisotropy.

Brain Research, 177 (1979) 61-82 ~(')Elsevier/North-Holland Biomedical Press 61 C O N D U C T I V I T Y IN T H E SOMATOSENSORY CORTEX OF THE CAT - E...
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