Download Three-dimensional reconstruction of the basket cell of the human

BraOt Research, 70 (1974) 511-514
C Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
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Three-dimensional reconstruction of the basket cell of the human motor
cortex
MIGUEL MARIN-PADILLA AND GEORGE R. STIBITZ
Departnwnts of Patholog), and Ph)'siolog3', Dartmouth Medical School, Hanover, N.H. 03755 (U.S.A.)
(Accepted January 21st, 1974)
The basket cell is a specialized interneuron of the human motor cortex which
forms pericellular baskets around the soma of the pyramidal neurons ~. This cell
appears to be spatially oriented in a specific manner within the motor cortex 3. The
study of rapid Golgi preparations has suggested that the basket cell is a fiat neuron
enclosed in its entirety within a narrow, by-and-large disc-shaped tissue volume oriented perpendicular to the pia mater and to the long axis of the precentral gyrus ~,4. The
basket cell can be visualized in its entirety only in preparations cut in that particular
plane; any change in the angle of view of this fiat neuron would change its morphological appearance. It has been postulated 5 that if this neuron were to be viewed 'in
profile' or in preparations cut parallel to the long axis of the precentral gyrus it would
have the appearance of a 'double-tufted' neuron. To pursue this suggestion we have
devised a model lbr a 3-dimensional reconstruction of the cortical basket cell utilizing
the computer and data (tomographic series of camera lucida drawings) obtained
from microscopic observations of rapid Golgi preparations.
Basket cells from layers If, upper Ill, lower Ill, IV and V were selected from
rapid Golgi preparations (cut perpendicular to the pia and to the long axis of the
precentral gyrus) of the motor cortex of a 2-month-old infant. A continuous camera
lucida drawing was made of each selected neuron to illustrate its morphological
appearance from that angle of view (Fig. 1). In addition, a series of separate camera
lucida drawings was made of each neuron by setting the microscope at various subsequent depths, such as 0, 5, 10, 1 5 . . . l~m from the surface of the preparation. At each
of these depths only those axonic and dendritic components of the selected neuron
which were in sharp focus were drawn. The number of steps (drawings) necessary to
draw a complete neuron represents the thickness of the cell as well as that of its territory of distribution.
The series of separate drawings of each neuron were reduced to numerical forms
by reading the (×, y) coordinates of numerous points along the cell arborizations.
These were entered into a computer file. The Dartmouth time-sharing system was
used, the central processing system of which is a GE (Honeywell) 635 processor. The
z value or depth of points read from each drawing were also entered. The computer
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traced all paths from the cell b o d y to terminal points, and a p p l i e d a s m o o t h i n g or
i n t e r p o l a t i n g f o r m u l a to points connected by segments o r branches so that they
extended s m o o t h l y from one depth to another. Finally, the c o m p u t e r p r o g r a m asked
the user to specify the p o i n t from which the neuron was to be viewed, and calculated
the c o o r d i n a t e s (u, v) o f the cell points as seen from the specified direction. The coinputer then plotted the segments o f branches o f the entire neuron.
The results pertaining to one o f the basket cells analyzed are r e p r o d u c e d herein
(Fig. 1). The m o r p h o l o g i c a l a p p e a r a n c e o f this neuron as it a p p e a r s in the Golgi
p r e p a r a t i o n s is illustrated by the c o n t i n u o u s c a m e r a lucida d r a w i n g o f it (Fig. 1). The
series o f c o m p u t e r r e p r o d u c t i o n s (Fig. I) o f this basket cell illustrates its changing
m o r p h o l o g i c a l a p p e a r a n c e as viewed from various angles such as: 0 °, 30", 40 °, 60",
70 '~, and 80" respectively. Pairs o f these plots at a n g u l a r s e p a r a t i o n o f a b o u t 10<~can be
viewed stereoscopically which will illustrate the t h r e e - d i m e n s i o n a l structural organization o f these neurons.
It is concluded that the basket cells o f the h u m a n m o t o r cortex are indeed, as
suggested previously, 'flat' neurons whose m o r p h o l o g i c a l a p p e a r a n c e changes as the
angle o f view changes. The basket cell when viewed 'in profile' assumes the a p p e a r a n c e
o f a ' d o u b l e - t u f t e d ' neuron. In this respect it should be pointed out that Cajal l, as it is
so often the case, recognized a variety a m o n g the ' d o u b l e - t u f t e d ' cells o f the h u m a n
m o t o r cortex which was characterized by the f o r m a t i o n o f axonal baskets a r o u n d the
s o m a o f p y r a m i d a l neurons. Cajal did not record the orientation o f his G o l g i p r e p a r a tions in that p a r t i c u l a r instance, but in view o f the findings presented here, it is p r o b a ble that this variety o f neurons represents basket cells a p p e a r i n g in profile in sections
oriented parallel to the long axis o f the precentral gyrus. It should be emphasized that
such flat neurons can be visualized in their entirety only in Golgi p r e p a r a t i o n s cut
parallel to the plane in which their dendrites are disposed. P r e p a r a t i o n s cut perpendicular to that plane can only d e m o n s t r a t e a p o r t i o n o f the neuron not thicker than the
150-200 #m which represent the thickness o f the section. The c o m p u t e r i z e d display
p r o c e d u r e here followed permits the complete visualization and reconstruction o f flat
n e u r o n s from any desired angle, s o m e t h i n g which could not be o b t a i n e d by simply
changing the orientation o f the G o l g i p r e p a r a t i o n .
Fig, 1. A: camera lucida drawing of a basket cell of the motor cortex (area 4) of a 2-month-old infant.
This cell is located 1200/ml from the pial surface in the upper region of layer V. It is a flat neuron
which measures approximately 800/~m in length, 650/;m in height and only 55 ,,m in thickness. This
neuron is enclosed in its entirety (receiving and emitting cell processes) within a thin rectangular
cortical tissue slice of similar dimensions which is oriented perpendicular to both the pia mater and the
long axis of the precentral gyrus. It should be pointed out that this basket cell and its territory of
distribution are enclosed inside a Golgi preparation which measures approximately 9,000 /;m in
length, 2,500/;m in height and 125/;m in thickness. 0 <: direct computer reconstruction of the basket
cell (A) from data obtained from the rapid Golgi preparation. 30° 70<': rotation of this basket cell
made by the computer illustrating the changing morphological appearance of this neuron as the angle
of view changes. 80': an almost edgewise view of this neuron illustrating its new appearance with
predominantly vertical dendritic and axonal arborizations. Observed at this angle the neuron is
morphologically indistinguishable from the 'double-tufted' neurons of the human motor cortex
described by Cajal 7 decades ago. Stereoscopic view of any pair of these computer drawings at an
angular separation of about 10' will visualize the 3-dimensional organization of these neurons.
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It is further concluded that perhaps other neurons which have been considered
as distinct types on the basis o f their morphological appearance may, in fact. t~e of the
same type but viewed differently. The spatial orientation of Gotgi preparations of the
cerebral cortex must always be determined and recorded, since the appearance o f the
fibrillar-neuronal structures may vary considerably depending upon the angle from
which they are examined. The changing appearance of several types of neuron in the
cerebellum when viewed from different angles is perhaps the best known example of
spatial orientation of the nerve elements within a nucleus and of its functional implications and significance.
A detailed study of the 3-dimensional organization (spatial orientation) of the
basket cells of layers 11, 1II, IV, and V to determine their overall territory of distribution within the human motor cortex is in preparation. It will include ~ complete
description of the computer model presented here and will explore its possible applications to the study of the spatial organization and the relationships between the
various fibrillar-neuronal structures of the human cerebral cortex.
This work was supported by Grant HD-03298 from the National institutes of
Health, U.S.A.
1 CAJAL,S. RAMONY, Histologie du Syst~me Nerveux de l'Homme et des Vert&brds, l~d. II, Maloine.
Paris, 1911, pp. 537-542.
2 MARIN-PADILLA,M., Origin of the pericellular baskets of the pyramidal cells of the human motor
cortex. A Golgi study, Brain Research, 14 (1969) 633-646.
3 MARIN-PADILLA,M., Prenatal and postnatal ontogenesis of the human motor cortex; A Golgi
study. If. The basket-pyramidal system, Brain Research, 23 (1970) 185-191.
4 MARIN-PADILLA,M., Double origin of the pericellular baskets of the pyramidal cellS of the human
motor cortex. A Golgi study, Brain Research, 38 (1972) 1-12.
5 MARIN-PADILLA,M., Development, structure and spatial orientation of the basket cells of the
human motor cortex, in P. RAKYC(Chairman), Local circuit neurons, Neuroseiences Res. Prog.
Bull,, MIT Press, Cambridge, Mass, in press.