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Autapses in neocortex cerebri: synapses between a pyramidal cell's axon and its own dendrites
355
BRAIN RESEARCH
Short Communications Autapses in neocortex cerebri: synapses between a pyramidal cell's axon and its own dendrites We propose the term 'autapse'* to describe a synapse between a neuron and a branch of its own axon. This report describes autapses between axon collaterals and branches of basal dendrites of pyramidal cells in cerebral neocortex. We found such synaptic arrangements - - the observation initially surprised us - - during a long-term quantitative analysis of cortical circuitry. The autapses were seen in Golgi preparations 2a of rabbit occipital cortex; this region of cortex encompasses both the area striata and the field between area striata and the posterior rhinal sulcus 17. The observations were made utilizing the highest resolution of the light microscope. Neuronal geometry was analyzed by a specially designed computer 6 which receives the outputs of linear displacement transducers signaling the positions, in x-, y- and z-coordinates, of the microscope stage. Using this 'computer microscope', the processes of 12 pyramidal cells were tracked in order to determine the connections of each of these neurons with other neurons. In Fig. 1, the computer trace of 1 of the 12 analyzed cells is shown. These cells - - deemed completely impregnated - - were taken from 5 animals and were located at various depths below the pial surface; their selection was not influenced by the presence of autapses. We found that 6 of these 12 nerve cells had autapses. One cell (neuron K-3 from which the illustrations to this paper have been derived) had 4 autapses, one had 3, three had 2, and one had 1 autapse. For sections of the thickness used in this study (100 #m) it has been calculated that only half of an average pyramidal cell's total length in dendrites is shown; the other half has been pruned away by the microtome knife z4. Therefore, a neuron may well have more autapses than we observed. Six of the 14 autapses observed were climbing fiber arrangements (each of them with multiple contacts; cJ:, e.g., Fig. 2b), 8 were 'punctiform'. The axonal components of the autapses observed were either boutons terminaux or boutons de passage. Twelve of the 14 dendritic components involved were dendrite branches of second, third, and fourth order (a second order branch connects the first bifurcation with the second, etc.). Fig. 2a presents a collage of photomicrographs of a complete 'autaptic loop'; two of its autapses are rendered in detail in Fig. 2b and c. The mean distance between axon origin and autapse, measured along the axon, is 169/zm (range 55-297/~m). The mean distance between autapse and axon origin, measured along dendrite branches and soma, is 103 # m (range 53-190/~m). The mean length of the autaptic loop is 272/~m (range 120--477/~m). In making these measure-
* From Gr. autos and haptein; cfi genesis of terms synapse5 and ephapset. Brain Research, 48 (1972) 355-360
356
SHORT
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Fig. 1. Computer-trace of a Golgi-lmpregnated autapse-bearing pyramidal cell of rabbit neocortex cerebri. Magnification x 325. From the cell body emanate: axon, rendered in continuous lines, basal dendrites 1 4 , rendered in stippled lines, and apical dendrite (ad), not traced. Synapses on dendrites made by axons of other Golgi-impregnated cells, are represented by O ; synapses made by the traced axon upon dendrites of other impregnated cells, by O. Arrows point to blackened circles which represent the autapses. All synapses represented by circles are 'punctiform'; those represented by the 'elongated' circles are 'climbing fiber' arrangements, one of which is an autapse on dendrite 4. The caliber of the neuron's processes is not depicted in the trace; neither are spines on dendrites, nor small beads on axons.
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SHORT COMMUNICATIONS
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Fig. 2. a, Collage of photomicrographs - - taken at various focal planes - - of neuron K-3. For computer trace and key see Fig. I. The 'autaptic loop' involving the proximal autapse on dendrite 3,~, and both autapses on dendrite 4,tt, is black. Other parts of the neuron are gray. (Collage made of 4 fully developed and of 2 underdeveloped photographs.) Magnification x 600. b, c, Details - - at x 1200 - - of two of the autapses presented in a. b is a collage of 6 photographs; the axon collateral is indicated by the two simple arrows; the autaptic climbing fiber arrangement on dendrite 4 (left ~' in a) is seen between two winged arrows, c is a collage of two photographs showing, at winged arrow, the punctiform autapse on dendrite 4 (right ~' in a).
m e n t s we used o u r c o m p u t e r microscope's capability of a p p r o x i m a t i n g the m e a n d e r i n g p a t t e r n o f the n e u r o n a l processes by straight segments 20-30 # m long. I n a n a t t e m p t to find classic descriptions of this peculiar, b u t possibly c o m m o n , synaptic (i.e. autaptic) a r r a n g e m e n t , we f o u n d a clear a c c o u n t by Held written in 18979. A partial q u o t e : ' T h e extraordinarily n u m e r o u s collaterals of a Purkinje cell axon end n o t only u p o n other Purkinje cells b u t also u p o n the cell of origin of the axon stem itself* . . . . I should like to designate these collaterals 'autocellular collaterals'.' (our translation). Held finds this a r r a n g e m e n t also in several nuclei cont a i n i n g lower m o t o r neurons. His well-reasoned speculations a b o u t the possible * Observed in adult human cerebellar cortex stained by a Golgi method.
Brain Research, 48 (1972) 355-360
358
SHORJ COMMUNICATIONS
functional significance of these arrangements include the notions that the pertinent neuron may be capable of 'self-excitation' and 'self-sensing'. CajaF' categorically rejects Held's findings. Subsequently, and apparently independently, autapses have been reported and depicted rarely3,18,19. Twice since Held have they been the object of a discourse (lengthy is, and brief 3) correlating structure and function. However, in these discussions it was not deemed significant that a neuron synaptically connect onto itself; it was only essential that neurons of a certain class connect to neurons of that same class. Observations of autapses in cerebral cortex were described and illustrated 19, or mentioned in passing is. Deserving special mention is Crain's discussion a of evoked depolarizing potentials which were recorded by him from cultured sensory ganglion cells. Crain speculates that these potentials may well be associated with morphologic arrangements such as described by, e.g. Nakai14: contacts between terminals of recurrent collaterals from cultured spinal ganglia cell axons, and the cell bodies from which the axons themselves had issued. These contacts may well be synapses: Crain correlates his findings with the recent electron microscopic observation 13 of axosomatic synapses in cultures of chick embryo spinal ganglia. in current neuronal circuit diagrams, autaptic arrangements do not appear; this absence is particularly noticeable in those diagrams which are made to illustrate neuronal feedback - - cf., e.g. Lorente de N612 (Figs. 2 and 12-1) and HorridgO ° (Fig. 14.11 *). interestingly, autaptic arrangements do occur in circuits incorporating neuromimes**. Harmon proposed such a circuit as early as 19617 (Fig. 8). For a more comprehensive treatment of 'closed-loop couplings' with 'self-inhibition', related to neurobiologic reality, c f Harmon s (Figs. 1A and 11). See also Taylor 21 (Figs. 7, 8, 12 and 24). We propose that the autapse may well be the substrate of a significant gating mechanism which puts part of the neuron's inputs under the control of the neuron's own output. According to this hypothesis, excitatory synaptic inputs from other cells on the dendrite segment distal to an autapse would have their influence at the neuron's impulse generating zone modified by that autapse. There are two assumptions underlying our hypothesis: (1) basal dendrites of neocortical pyramids conduct only passively; (2) autapses are inhibitory***. According to RalP 5, dendritic synaptic excitation is especially vulnerable to synaptic inhibition of the same dendritic location. Fig. 3 gives a schematic representation of our gating hypothesis. If this gating hypothesis can be accepted, an interesting question may be posed : is there something qualitatively different about the input to that part of the autaptic * The circuit evolved by Horridge contains a closed neuronal loop with presynaptic inhibition. However, according to the author, the mechanism proposed could just as well operate on the basis of a loop incorporating postsynaptic inhibition. ** 'Neuromime' - - a term which might be more frequently applied so as to avoid confusion - - was proposed by Van Bergeijk~2 to denote a neuron-model, i.e. an artificial neuron. * ** This suggests the idea that autaptic neurons may be inhibitory at all their terminals. If assumptions (1) and (2) do not apply - - i.e., if dendrites conduct actively (by retrograde spike-invasion or otherwise) and/or if autapses are excitatory - - then the role of autapses would be quite different. A formulation of alternative hypotheses is beyond the scope of this paper. Brain Research, 48 (1972) 355-360
359
SHORT COMMUNICATIONS
Fig. 3. Excitatory membrane changes, set up in dashed part of basal dendrite tree of cortical pyramid, have their influence on the impulse-generating zone i modified by the inhibitory conductance change which is delivered by autapse a. In other words: inputs 42,are autaptically gated; inputs ~ . a r e unaffected by activity of autapse a.
cell's dendrite tree which is distal to the autapse? Should this be so, one may argue, a discrete part of the cell's input (e.g., input from a specific set of neurons) is autaptically gated. It should be of great interest to estimate the occurrence of autapses in various neuron classes, and in various regions of nervous systems. In a preliminary survey, we found autapses in cerebral neocortices of a variety of other species. It is particularly important that the existence of the autapse be confirmed at the ultrastructural level and, if confirmed, that its morphologic characteristics be further elucidated. For such a study, Golgi-EM combination methods, which were developed and successfully applied by e.g. Stell 2° and Kolb 11, will have to be modified: the fact that both axon and dendrite engaging in an autapse are Golgi-positive, calls for a technique which leaves Golgi-impregnated elements with acceptable cytologic preservation. Here, Richardson's recent EM studies of methylene-blue stained neural elements16 may hold promise. We thank Drs. Mark E. Molliver, John C. Hedreen (Johns Hopkins Univ.) and Thomas A. Woolsey (Washington Univ.) for critically reading, and commenting upon, the manuscript. We are grateful to many of our colleagues for valuable discussions; in particular, we thank Drs. W. Rall (N.I.H.), J. Del Castillo (Univ. Puerto Rico), G. Poggio and I. Darian-Smith (Johns Hopkins Univ.), and members of the Department of Neurobiology (Harvard Univ.). This work is supported by Grants from the U.S. Public Health Service (NS 04012 and NS 07773) and from the Joseph P. Kennedy, Jr., Memorial Foundation. Department of Anatomy, The Johns Hopkins University School of Medicine, Baltimore, Md. 21205, and Department of Physiology, University of Maryland School of Medicine, Baltimore, Md. 21201 (U.S.A.)
H E N D R I K VAN DER LOOS*
E D M U N D M. GLASER
* Senior Research Scholar of the Joseph P. Kennedy, Jr., Memorial Foundation.
Brain Research, 48 (1972) 355-360
360
SHORT COMMUNICATIONS
1 ARVANITAKI,A., Effects evoked in an axon by the activity of a contiguous one, J. Neurophysiol.. 5 (1942) 89-108. 2 CAJAL,S. RAMBNY, Histologie du Systdme Nerveux de l'Homme et des Vertdbrds. Tome 2, Maloine, Paris, 1911, p. 18. 3 CHAN-PALAY,V., The recurrent collaterals of Purkinje cell axons: a correlated study of the rat's cerebellar cortex with electron microscopy and the Golgi method, Z. Anat. Entwickl.-Gesch., 134 (1971) 200-234. 4 CRAIN, S. M., Intracellular recordings suggesting synaptic functions in chick embryo spinal sensory ganglion cells isolated in vitro, Brain Research, 26 (1971) 188-191. 5 FOSTER,M., AND SHERRINGTON,C. S., A Textbook of Physiology, Part III: The Central Nervous System, MacMillan, London, 1897, p. 929. 6 GLASER,E. M., AND VAN DER LOPS, H., A semi-automatic computer-microscope for the analysis of neuronal morphology, IEEE Trans. bio-med. Engn., BME-12 (1965) 22-31. 7 HARMON,L. D., Studies with artificial neurons, I : Properties and functions of an artificial neuron, Kybernetik, 1 (1961)89-101. 8 HARMON,L. D., Modeling studies of neural inhibition. In C. YON EULER, S. SKOGLUNDAND U. S6DERBERG(Eds.), Structure and Function of Inhibitory Neuronal Mechanisms, Pergamon, Oxford, 1968, pp. 537-563. 9 HELD, H., Beitr~ige zur Structur der Nervenzellen und ihrer Forts/itze, 2. Abh., Arch. Anat. Physiol. (Lpz.), Anat. Abt., (1897) 204-294. 10 HORRIDGE,G. A., lnterneurons, their Origin, Action, Specificity, Growth and Plasticity, Freeman, London, 1968, p. 367. 11 KOLB, H., Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells, Phil. Trans. B, 258 (1970) 261-283. 12 LORENTEDE N6, R., Analysis of the activity of the chains of internuncial neurons, J. Physiol. (Lond.), 1 (1938)207-244. 13 MILLER, R., VARON,S., KRUGER,L., COATES,P. W., AND ORKAND,P. M., Formation of synaptic contacts in dissociated chick embryo sensory ganglion cells in vitro, Brain Research, 24 (1970) 356-358. 14 NArCAI,J., Dissociated dorsal root ganglia in tissue culture, Amer. J. Anat., 99 (1956) 81-130. 15 RALL, W., Cable properties of dendrites and effects of synaptic location. In P. ANDERSENAND J. K. S. JANSEN (Eds.), Excitatory Synaptic Mechanisms, Universitetsforlaget, Oslo, 1970, pp. 175-188. 16 RICHARDSON,K. C., The fine structure of autonomic nerves after vital staining with methylene blue, Anat. Rec., 164 (1969)359-378. 17 ROSE, M., Zytoarchitektonischer Atlas der Grosshirnrinde des Kaninchens, J. Psychol. Neurol. (Lpz.), 43 (1931) 353-440. 18 SCHEIBEL, M. E., AND SCHEIBEL,A. B., Inhibition and the Renshaw cell. A structural critique, Brain Behav. Evol., 4 (1971) 53-93. 19 SHKOL'NIK-YARROS,E. G., Neurons and Interneuronal Connections of the Central Visual System, Plenum Press, New York, 1971, p. 154. 20 STELE, W. K., Correlation of retinal cytoarchitecture and ultrastructure in Golgi preparations, Anat. Rec., 153 (1965) 389-398. 21 TAYLOR,W. K., A model of learning mechanisms in the brain. In N. WIENERAND J. P. SCHAD/~ (Eds.), Cybernetics of the Nervous System, Progress in Brain Research, 1Iol. 17, Elsevier, Amsterdam, 1965, pp. 369-397. 22 VAN BERGEIJK, W. A., Nomenclature of devices which simulate biological functions, Science, 132 (1960) 1248-1249. 23 VAN DER LOPS, H., Dendro-dendritische Verbindingen in de Schors der Grote Hersenen, Stare, Haarlem, 1959, Ch. IIb. (English translation of protocol of modified Golgi-Cox method available upon request.) 24 VAN DER LOPS, H., On dendro-dendritic junctions in the cerebral cortex. In D. B. TOWER AND J. P. SCHADI~(Eds.), Structure and Function of the Cerebral Cortex, Elsevier, Amsterdam, 1960, pp. 36-42. (Accepted August 31st, 1972)
Brain Research, 48 (1972) 355-360
BRAIN RESEARCH
Short Communications Autapses in neocortex cerebri: synapses between a pyramidal cell's axon and its own dendrites We propose the term 'autapse'* to describe a synapse between a neuron and a branch of its own axon. This report describes autapses between axon collaterals and branches of basal dendrites of pyramidal cells in cerebral neocortex. We found such synaptic arrangements - - the observation initially surprised us - - during a long-term quantitative analysis of cortical circuitry. The autapses were seen in Golgi preparations 2a of rabbit occipital cortex; this region of cortex encompasses both the area striata and the field between area striata and the posterior rhinal sulcus 17. The observations were made utilizing the highest resolution of the light microscope. Neuronal geometry was analyzed by a specially designed computer 6 which receives the outputs of linear displacement transducers signaling the positions, in x-, y- and z-coordinates, of the microscope stage. Using this 'computer microscope', the processes of 12 pyramidal cells were tracked in order to determine the connections of each of these neurons with other neurons. In Fig. 1, the computer trace of 1 of the 12 analyzed cells is shown. These cells - - deemed completely impregnated - - were taken from 5 animals and were located at various depths below the pial surface; their selection was not influenced by the presence of autapses. We found that 6 of these 12 nerve cells had autapses. One cell (neuron K-3 from which the illustrations to this paper have been derived) had 4 autapses, one had 3, three had 2, and one had 1 autapse. For sections of the thickness used in this study (100 #m) it has been calculated that only half of an average pyramidal cell's total length in dendrites is shown; the other half has been pruned away by the microtome knife z4. Therefore, a neuron may well have more autapses than we observed. Six of the 14 autapses observed were climbing fiber arrangements (each of them with multiple contacts; cJ:, e.g., Fig. 2b), 8 were 'punctiform'. The axonal components of the autapses observed were either boutons terminaux or boutons de passage. Twelve of the 14 dendritic components involved were dendrite branches of second, third, and fourth order (a second order branch connects the first bifurcation with the second, etc.). Fig. 2a presents a collage of photomicrographs of a complete 'autaptic loop'; two of its autapses are rendered in detail in Fig. 2b and c. The mean distance between axon origin and autapse, measured along the axon, is 169/zm (range 55-297/~m). The mean distance between autapse and axon origin, measured along dendrite branches and soma, is 103 # m (range 53-190/~m). The mean length of the autaptic loop is 272/~m (range 120--477/~m). In making these measure-
* From Gr. autos and haptein; cfi genesis of terms synapse5 and ephapset. Brain Research, 48 (1972) 355-360
356
SHORT
COMMUNICATIONS
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•
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axon
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NEURON K - 3
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Fig. 1. Computer-trace of a Golgi-lmpregnated autapse-bearing pyramidal cell of rabbit neocortex cerebri. Magnification x 325. From the cell body emanate: axon, rendered in continuous lines, basal dendrites 1 4 , rendered in stippled lines, and apical dendrite (ad), not traced. Synapses on dendrites made by axons of other Golgi-impregnated cells, are represented by O ; synapses made by the traced axon upon dendrites of other impregnated cells, by O. Arrows point to blackened circles which represent the autapses. All synapses represented by circles are 'punctiform'; those represented by the 'elongated' circles are 'climbing fiber' arrangements, one of which is an autapse on dendrite 4. The caliber of the neuron's processes is not depicted in the trace; neither are spines on dendrites, nor small beads on axons.
"
SHORT COMMUNICATIONS
357
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Fig. 2. a, Collage of photomicrographs - - taken at various focal planes - - of neuron K-3. For computer trace and key see Fig. I. The 'autaptic loop' involving the proximal autapse on dendrite 3,~, and both autapses on dendrite 4,tt, is black. Other parts of the neuron are gray. (Collage made of 4 fully developed and of 2 underdeveloped photographs.) Magnification x 600. b, c, Details - - at x 1200 - - of two of the autapses presented in a. b is a collage of 6 photographs; the axon collateral is indicated by the two simple arrows; the autaptic climbing fiber arrangement on dendrite 4 (left ~' in a) is seen between two winged arrows, c is a collage of two photographs showing, at winged arrow, the punctiform autapse on dendrite 4 (right ~' in a).
m e n t s we used o u r c o m p u t e r microscope's capability of a p p r o x i m a t i n g the m e a n d e r i n g p a t t e r n o f the n e u r o n a l processes by straight segments 20-30 # m long. I n a n a t t e m p t to find classic descriptions of this peculiar, b u t possibly c o m m o n , synaptic (i.e. autaptic) a r r a n g e m e n t , we f o u n d a clear a c c o u n t by Held written in 18979. A partial q u o t e : ' T h e extraordinarily n u m e r o u s collaterals of a Purkinje cell axon end n o t only u p o n other Purkinje cells b u t also u p o n the cell of origin of the axon stem itself* . . . . I should like to designate these collaterals 'autocellular collaterals'.' (our translation). Held finds this a r r a n g e m e n t also in several nuclei cont a i n i n g lower m o t o r neurons. His well-reasoned speculations a b o u t the possible * Observed in adult human cerebellar cortex stained by a Golgi method.
Brain Research, 48 (1972) 355-360
358
SHORJ COMMUNICATIONS
functional significance of these arrangements include the notions that the pertinent neuron may be capable of 'self-excitation' and 'self-sensing'. CajaF' categorically rejects Held's findings. Subsequently, and apparently independently, autapses have been reported and depicted rarely3,18,19. Twice since Held have they been the object of a discourse (lengthy is, and brief 3) correlating structure and function. However, in these discussions it was not deemed significant that a neuron synaptically connect onto itself; it was only essential that neurons of a certain class connect to neurons of that same class. Observations of autapses in cerebral cortex were described and illustrated 19, or mentioned in passing is. Deserving special mention is Crain's discussion a of evoked depolarizing potentials which were recorded by him from cultured sensory ganglion cells. Crain speculates that these potentials may well be associated with morphologic arrangements such as described by, e.g. Nakai14: contacts between terminals of recurrent collaterals from cultured spinal ganglia cell axons, and the cell bodies from which the axons themselves had issued. These contacts may well be synapses: Crain correlates his findings with the recent electron microscopic observation 13 of axosomatic synapses in cultures of chick embryo spinal ganglia. in current neuronal circuit diagrams, autaptic arrangements do not appear; this absence is particularly noticeable in those diagrams which are made to illustrate neuronal feedback - - cf., e.g. Lorente de N612 (Figs. 2 and 12-1) and HorridgO ° (Fig. 14.11 *). interestingly, autaptic arrangements do occur in circuits incorporating neuromimes**. Harmon proposed such a circuit as early as 19617 (Fig. 8). For a more comprehensive treatment of 'closed-loop couplings' with 'self-inhibition', related to neurobiologic reality, c f Harmon s (Figs. 1A and 11). See also Taylor 21 (Figs. 7, 8, 12 and 24). We propose that the autapse may well be the substrate of a significant gating mechanism which puts part of the neuron's inputs under the control of the neuron's own output. According to this hypothesis, excitatory synaptic inputs from other cells on the dendrite segment distal to an autapse would have their influence at the neuron's impulse generating zone modified by that autapse. There are two assumptions underlying our hypothesis: (1) basal dendrites of neocortical pyramids conduct only passively; (2) autapses are inhibitory***. According to RalP 5, dendritic synaptic excitation is especially vulnerable to synaptic inhibition of the same dendritic location. Fig. 3 gives a schematic representation of our gating hypothesis. If this gating hypothesis can be accepted, an interesting question may be posed : is there something qualitatively different about the input to that part of the autaptic * The circuit evolved by Horridge contains a closed neuronal loop with presynaptic inhibition. However, according to the author, the mechanism proposed could just as well operate on the basis of a loop incorporating postsynaptic inhibition. ** 'Neuromime' - - a term which might be more frequently applied so as to avoid confusion - - was proposed by Van Bergeijk~2 to denote a neuron-model, i.e. an artificial neuron. * ** This suggests the idea that autaptic neurons may be inhibitory at all their terminals. If assumptions (1) and (2) do not apply - - i.e., if dendrites conduct actively (by retrograde spike-invasion or otherwise) and/or if autapses are excitatory - - then the role of autapses would be quite different. A formulation of alternative hypotheses is beyond the scope of this paper. Brain Research, 48 (1972) 355-360
359
SHORT COMMUNICATIONS
Fig. 3. Excitatory membrane changes, set up in dashed part of basal dendrite tree of cortical pyramid, have their influence on the impulse-generating zone i modified by the inhibitory conductance change which is delivered by autapse a. In other words: inputs 42,are autaptically gated; inputs ~ . a r e unaffected by activity of autapse a.
cell's dendrite tree which is distal to the autapse? Should this be so, one may argue, a discrete part of the cell's input (e.g., input from a specific set of neurons) is autaptically gated. It should be of great interest to estimate the occurrence of autapses in various neuron classes, and in various regions of nervous systems. In a preliminary survey, we found autapses in cerebral neocortices of a variety of other species. It is particularly important that the existence of the autapse be confirmed at the ultrastructural level and, if confirmed, that its morphologic characteristics be further elucidated. For such a study, Golgi-EM combination methods, which were developed and successfully applied by e.g. Stell 2° and Kolb 11, will have to be modified: the fact that both axon and dendrite engaging in an autapse are Golgi-positive, calls for a technique which leaves Golgi-impregnated elements with acceptable cytologic preservation. Here, Richardson's recent EM studies of methylene-blue stained neural elements16 may hold promise. We thank Drs. Mark E. Molliver, John C. Hedreen (Johns Hopkins Univ.) and Thomas A. Woolsey (Washington Univ.) for critically reading, and commenting upon, the manuscript. We are grateful to many of our colleagues for valuable discussions; in particular, we thank Drs. W. Rall (N.I.H.), J. Del Castillo (Univ. Puerto Rico), G. Poggio and I. Darian-Smith (Johns Hopkins Univ.), and members of the Department of Neurobiology (Harvard Univ.). This work is supported by Grants from the U.S. Public Health Service (NS 04012 and NS 07773) and from the Joseph P. Kennedy, Jr., Memorial Foundation. Department of Anatomy, The Johns Hopkins University School of Medicine, Baltimore, Md. 21205, and Department of Physiology, University of Maryland School of Medicine, Baltimore, Md. 21201 (U.S.A.)
H E N D R I K VAN DER LOOS*
E D M U N D M. GLASER
* Senior Research Scholar of the Joseph P. Kennedy, Jr., Memorial Foundation.
Brain Research, 48 (1972) 355-360
360
SHORT COMMUNICATIONS
1 ARVANITAKI,A., Effects evoked in an axon by the activity of a contiguous one, J. Neurophysiol.. 5 (1942) 89-108. 2 CAJAL,S. RAMBNY, Histologie du Systdme Nerveux de l'Homme et des Vertdbrds. Tome 2, Maloine, Paris, 1911, p. 18. 3 CHAN-PALAY,V., The recurrent collaterals of Purkinje cell axons: a correlated study of the rat's cerebellar cortex with electron microscopy and the Golgi method, Z. Anat. Entwickl.-Gesch., 134 (1971) 200-234. 4 CRAIN, S. M., Intracellular recordings suggesting synaptic functions in chick embryo spinal sensory ganglion cells isolated in vitro, Brain Research, 26 (1971) 188-191. 5 FOSTER,M., AND SHERRINGTON,C. S., A Textbook of Physiology, Part III: The Central Nervous System, MacMillan, London, 1897, p. 929. 6 GLASER,E. M., AND VAN DER LOPS, H., A semi-automatic computer-microscope for the analysis of neuronal morphology, IEEE Trans. bio-med. Engn., BME-12 (1965) 22-31. 7 HARMON,L. D., Studies with artificial neurons, I : Properties and functions of an artificial neuron, Kybernetik, 1 (1961)89-101. 8 HARMON,L. D., Modeling studies of neural inhibition. In C. YON EULER, S. SKOGLUNDAND U. S6DERBERG(Eds.), Structure and Function of Inhibitory Neuronal Mechanisms, Pergamon, Oxford, 1968, pp. 537-563. 9 HELD, H., Beitr~ige zur Structur der Nervenzellen und ihrer Forts/itze, 2. Abh., Arch. Anat. Physiol. (Lpz.), Anat. Abt., (1897) 204-294. 10 HORRIDGE,G. A., lnterneurons, their Origin, Action, Specificity, Growth and Plasticity, Freeman, London, 1968, p. 367. 11 KOLB, H., Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells, Phil. Trans. B, 258 (1970) 261-283. 12 LORENTEDE N6, R., Analysis of the activity of the chains of internuncial neurons, J. Physiol. (Lond.), 1 (1938)207-244. 13 MILLER, R., VARON,S., KRUGER,L., COATES,P. W., AND ORKAND,P. M., Formation of synaptic contacts in dissociated chick embryo sensory ganglion cells in vitro, Brain Research, 24 (1970) 356-358. 14 NArCAI,J., Dissociated dorsal root ganglia in tissue culture, Amer. J. Anat., 99 (1956) 81-130. 15 RALL, W., Cable properties of dendrites and effects of synaptic location. In P. ANDERSENAND J. K. S. JANSEN (Eds.), Excitatory Synaptic Mechanisms, Universitetsforlaget, Oslo, 1970, pp. 175-188. 16 RICHARDSON,K. C., The fine structure of autonomic nerves after vital staining with methylene blue, Anat. Rec., 164 (1969)359-378. 17 ROSE, M., Zytoarchitektonischer Atlas der Grosshirnrinde des Kaninchens, J. Psychol. Neurol. (Lpz.), 43 (1931) 353-440. 18 SCHEIBEL, M. E., AND SCHEIBEL,A. B., Inhibition and the Renshaw cell. A structural critique, Brain Behav. Evol., 4 (1971) 53-93. 19 SHKOL'NIK-YARROS,E. G., Neurons and Interneuronal Connections of the Central Visual System, Plenum Press, New York, 1971, p. 154. 20 STELE, W. K., Correlation of retinal cytoarchitecture and ultrastructure in Golgi preparations, Anat. Rec., 153 (1965) 389-398. 21 TAYLOR,W. K., A model of learning mechanisms in the brain. In N. WIENERAND J. P. SCHAD/~ (Eds.), Cybernetics of the Nervous System, Progress in Brain Research, 1Iol. 17, Elsevier, Amsterdam, 1965, pp. 369-397. 22 VAN BERGEIJK, W. A., Nomenclature of devices which simulate biological functions, Science, 132 (1960) 1248-1249. 23 VAN DER LOPS, H., Dendro-dendritische Verbindingen in de Schors der Grote Hersenen, Stare, Haarlem, 1959, Ch. IIb. (English translation of protocol of modified Golgi-Cox method available upon request.) 24 VAN DER LOPS, H., On dendro-dendritic junctions in the cerebral cortex. In D. B. TOWER AND J. P. SCHADI~(Eds.), Structure and Function of the Cerebral Cortex, Elsevier, Amsterdam, 1960, pp. 36-42. (Accepted August 31st, 1972)
Brain Research, 48 (1972) 355-360