Comprehensive Physiology Wiley Online Library

Specificity of Neurons and their Interconnections

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Individuality of Nerve Cells and the Precision of Connections
1.1 Invertebrates
1.2 Vertebrates
2 Genetic Approaches to Connectivity and Nerve Function
2.1 Development Without Experience
2.2 Precision of Connectivity in Genetically Identical Organisms
2.3 Mutant Analysis
3 Experimental Analysis of the Specification of Connections
3.1 Examples of Nonspecific Synapse Formation
3.2 Specificity of Neuromuscular Connectivity in Vertebrates
3.3 Specification of Properties of Neuromuscular Connections and Their Regeneration in Invertebrates
3.4 Specificity of Regeneration of Sensory Nerves to Peripheral Structures
3.5 Specificity of Regeneration of Retinotectal Connections in Lower Vertebrates
4 Plasticity in Connectivity; Critical Periods
4.1 Effects of Visual Deprivation
4.2 Critical Period
4.3 Evidence for Competition Between Lateral Geniculate Neurons
4.4 Role of Experience in Development
4.5 Function of the Critical Period
4.6 Xenopus Ipsilateral Projection
4.7 Theoretical Need for Coherence of Activity
4.8 Morphological Correlates of Deprivation and Plasticity
5 Chemoaffinity and the Specificity of Neural Development and Regeneration
5.1 Gradients and Developmental Timing
5.2 Tissue Culture Approaches
5.3 Electron‐microscopic Reconstruction of Development and Glial Guidance
5.4 Chemical Interactions Governing Differentiation
5.5 Cell‐specific Macromolecules and Selective Adhesion
6 Summary
Figure 1. Figure 1.

A: photomicrograph of leech segmental ganglion, viewed from its ventral aspect. A few of the individually recognizable cells are labeled: T, touch cells; P, pressure cells; N, cells responsive only to noxious stimuli; R, giant Retzius cells; L, longitudinal motoneurons; A, annulus erector motoneurons, Con, connectives to adjacent ganglion.

From Nicholls & Baylor . B: diagrammatic representation of the skin receptive fields of different leech ganglia, sensory cells, and anterior (A) and posterior (P) ganglionic roots. Territory innervated by ganglion 2 (7 annuli) is heavily outlined. Note partial overlap of the fields of each ganglion. •, sensillae in the central annulus of each field. From Baylor & Nicholls
Figure 2. Figure 2.

Profiles of individual neurons, within ganglia, revealed by Procion yellow injection. A: leech ganglion touch cell; fine synaptic terminals in the ganglionic neuropile and axonal branches entering the anterior and posterior roots (to right) and running toward the anterior and posterior connections are shown.

From van Essen . B: F3 flexor motoneuron of a crayfish. From Selverston & Kennedy
Figure 3. Figure 3.

Segregation of inputs onto a hippocampal pyramidal neuron (A) and a layer V cerebral cortical pyramidal cell (B). In A, the predominant synaptic inputs at each location are a) collaterals of afferent fibers from outside the hippocampus, b) Schaeffer collaterals, c) septal afferents, d) mossy fibers, e) basket cell terminals, f) collaterals from other pyramidal cells. In B, inputs are a) nonspecific thalamic and reticular formation axons, b) specific afferent radiation (geniculocalcarine radiation), c) contralateral afferents, d) axons of nearby stellate cells, e) recurrent collaterals of other pyramidal cells

From Scheibel & Scheibel
Figure 4. Figure 4.

Auditory nerve fibers near their points of termination in the cochlear nucleus. Each fiber ends in several different parts of the nucleus with grossly different terminal morphology. The fibers shown are branching to end in the anteroventral (top) and posteroventral regions (bottom) of the cochlear nucleus

From Ramón y Cajal
Figure 5. Figure 5.

Electromyograms of 4 pairs of homologous flexor (Fl.) and extensor (Ext.) muscles in a normal (N) limb and a supernumerary (T) limb receiving input predominantly from one branch of the fifth spinal nerve. Although the patterns of activity are often quite similar, in other cases the homologous muscles act totally asynchronously

From Czéh & Székely
Figure 6. Figure 6.

Displacement of inappropriate nerve from a cross‐innervated fish eye muscle. Experimental design is shown at top. Superior oblique muscle (S‐O) was denervated near the cord, while the inferior oblique muscle (I‐O) was removed, leaving the I‐O nerve near the denervated S‐O muscle. Degree of rotation of the eye (vertical axis) to compensate for rotation of the body (horizontal axis) is shown below. ○, unoperated left eye; •, right eye immediately after operation; Δ, right eye 2 wk later, with S‐O muscle innervated by the I‐O nerve; •, right eye 6 wk later, after S‐O nerve had regrown into muscle

From Marotte & Mark
Figure 7. Figure 7.

Spread of peripheral motor fields and repression of synapses in axolotl limbs. Each pair of limbs represents the hindlimbs of an experimental animal in which the right limb shows normal innervation by spinal nerves 15 (lines slanting down to right), 16 (dots), and 17 (lines slanting down to left). The dark area in the right limb, top, represents innervation by both spinal nerves 15 and 16. The motor fields differ slightly from animal to animal but are normally quite symmetrical in a given individual. In the animal shown at top, nerve 16 in the left limb was denervated 7 days before testing. Already the fields of nerves 15 and 17 had expanded near the base of the limb, and there were patches of innervated fibers in the midst of still denervated fibers further distally. After 2–3 wk, the entire limb is innervated by nerves 15 and 17. After 1–2 months, however, nerve 16 regrows into the muscle and reasserts control of its original territory. If, in such an animal, nerve 16 is again sectioned and the motor fields tested only 3 days later (below), all the territory of nerve 16 is well innervated by terminals of nerves 15 and 17

From Cass et al.
Figure 8. Figure 8.

The frog retinotectal projection, as determined by morphological and electrophysiological investigations

From Jacobson , reprinted by permission of Holt, Rinehart and Winston, Inc
Figure 9. Figure 9.

Regrowth pattern of goldfish optic nerve fibers following partial ablation of the retina and section of the optic nerve. M and L, medial and lateral bundles, respectively, entering tectum; A, P, D, and V, anterior, posterior, dorsal, and ventral poles, respectively, of retina

From Attardi & Sperry
Figure 10. Figure 10.

Projection patterns of optic nerve fibers in intact goldfish (A) and after regeneration following partial tectal ablation. In all cases, a microelectrode was moved from point to point on the surface of the tectum and the locations of receptive fields in the contralateral retina determined. Note that, as in Fig. , the nasal‐temporal retinal axis is mapped on the rostral‐caudal axis of the tectum, the superior‐inferior retinal axis in the medial‐lateral dimension of the tectum. In B, the retina shows a compressed projection onto the half‐tectum remaining after ablation. In C, part of the projection is compressed in each axis, part is normal

From Yoon
Figure 11. Figure 11.

Parallel and overlapping retinotectal projection from compound eyes. At top the normal projection is shown, with nasal retina indicated by solid lines, temporal retina by broken lines. In the compound eyes, the projection from each half‐retina is expanded to fill the whole tectum, and the duplicated half‐retina projects to the tectum in a way appropriate to its original location but not to its final location in the eye

From Gaze
Figure 12. Figure 12.

Geniculocortical projections in normal and Siamese cats. In the latter, there is abnormal contralateral input to the geniculate (hatched area), and the resultant output to the visual cortex, representing about 20° of central retinal visual field that would normally go to the opposite side of the brain, now projects to both areas 17 and 18, displacing the normal inputs. At the border between areas 17 and 18, the projection now starts at −20°, rather than at 0°, and progresses through the midline (black area) and then across the part of the retina normally supplying it. The unshaded area on either side of the abnormal projection indicates regions where binocularity of input to cortical cells is lost

From Hubel & Wiesel
Figure 13. Figure 13.

Inferred organization of the visual cortex of a macaque monkey. In one dimension, alternating ocular dominance columns receive input from different layers of the lateral geniculate and are driven by closely corresponding points on the 2 retinas. Perpendicular to the ocular dominance columns are a larger number of orientation‐selective columns. Lateral interaction between ocular dominance columns at layers superficial and deep to layer IV account for the predominance of binocular driving at these other layers. c, contralateral; i, ipsilateral

From Hubel & Wiesel
Figure 14. Figure 14.

A: critical period for the establishment of binocular driving of cortical cells. Each histogram represents the number of cells studied that showed different degrees of ocular dominance ranging from total contralateral dominance (group 1) to total ipsilateral dominance (group 7). Group 2 shows marked contralateral dominance and group 3 slight contralateral dominance; in group 4 both eyes are equally effective. Histogram i was obtained from a 3–4‐wk‐old kitten with normal visual experience; the pattern would be essentially the same if the kitten had had no visual experience. Histogram ii was derived from a kitten with the contralateral eyelid sutured closed between days 23 and 29; the lack of patterned input from that eye, during that period, resulted in total loss of effectiveness of the inputs from that eye. In histogram iii, contralateral blindfolding between approximately days 65 and 100 was much less effective in reducing contralateral driving; the effect of monocular deprivation was essentially gone with suturing after the third or fourth month (histogram iv).

From Hubel & Wiesel .] B: comparable effect of strabismus during the critical period. Experimental kittens (histogram B) had their right medial rectus muscle cut before their eyes opened, so that the 2 eyes each had visual experience but no longer fixated simultaneously on the same points in space. Animals so treated, after 3–12 mo, showed a severe loss of binocular driving of cortical neurons. Histogram B shows the results for all cells studied, compared with the dominance pattern of cells in the control animals (histogram A). [From Hubel & Wiesel
Figure 15. Figure 15.

Experimental scheme used to test competition between lateral geniculate cells in maintaining functional cortical connections. The left eye was sutured closed, causing visual deprivation in lamina A (the top layer) of the contralateral lateral geniculate nucleus (LGN). When the right eye is intact, this results in cell shrinkage in segments 2–4 (shaded area), which overlap in cortical projection with output from layer A1 (below). Segment 1, which is equally deprived but does not overlap in its projection, shows less or no atrophy. To test whether competitive interaction at the level of the cortex is involved, area 3 of the right retina was destroyed, eliminating input to segment 3 of layer A1. In this case, there was atrophy of the cells in segment 3 of layer A1, and reduced atrophy in segment 3 of layer A

From Guillery
Figure 16. Figure 16.

Experimental design and results showing plasticity of connectivity during the critical period in kittens. Kittens, wearing a ruff to prevent vision of themselves, were placed in a plastic tube and exposed only to vertical stripes (as shown) or only to horizontal stripes for several hours each day. This was their only visual experience. Shown below are the orientation specificities of all the cortical neurons studied in cats so treated. In the horizontally experienced cat (left), all cells showed a preference for horizontally oriented stimuli; all cells tested in the vertically experienced cat (right) preferred vertically oriented stimuli. Control animals show approximately equal numbers of cells preferring all orientations

From Blakemore & Cooper
Figure 17. Figure 17.

Number of apical dendritic spines on layer V pyramidal cortical cells in visual cortex of normal and visually deprived mice. A shows the increase in number of spines per 100‐μm segment of apical dendrite (see inset C) in mice raised with normal visual experience, in the dark, and for 20 days in the dark followed by exposure to normal lighting. The derivative of each curve is shown in B, and the numbers of experimental animals used for each point is indicated in the area between A and B. Total light deprivation caused marked retardation of synaptic spine development, while exposure to light after 20 days led to rapid recovery to the normal numbers

From Valverde
Figure 18. Figure 18.

Increase in number of synapses (S) by a single nerve terminal on 2 or more dendritic spines per 100 single synaptic contacts (multiple synaptic index) as a function of time after incomplete lesion of the fimbrial input to hippocampal neurons. Within 2 to 3 days after the lesion, there is a large peak in the number of degenerating synapses, followed by a gradual disappearance of degenerating terminals over a period of approximately 30 days. During these 30 days, there is a striking increase in the number of synapses by one nerve terminal on 2 or more spines. The proposed explanation for this phenomenon is that nerve fibers that remain following the lesion sprout collaterals that innervate nearby vacated spines (see inset). S, dendritic spine; D, degenerating terminal; N, normal terminal

From Raisman & Field
Figure 19. Figure 19.

Glial guidance of migrating neurons. Temporal and spatial reconstruction of the developing cerebellar cortex showing different stages in the migration of granule cells (D) along the Bergmann glial fiber (BGF) processes of Golgi epithelial cells (GEC), from the surface of the cerebellum through the parallel fibers (PF) and past the stellate cells (S) and Purkinje cells (PC) to their eventual location. The orientation of the various planes is indicated by the geometric figure at lower left: transverse (I) and longitudinal (II) to the folium and parallel to the pial surface (III). Diameters of cellular elements are exaggerated for purposes of illustration. MF, mossy fiber; CF, climbing fiber; SD, stellate cell dendrite; EG, external granular cell layer; M, molecular layer; P, Purkinje cell layer; G, granular layer

From Rakic & Sidman
Figure 20. Figure 20.

Patterned reaggregation of dissociated hippocampal cells. A: section through intact mouse hippocampus at 19 days gestation. The prominent curved lamina of pyramidal cells is conspicuous, as is the compact dentate gyrus at bottom center. B: an aggregate of hippocampal cells dissociated at 18.5 days gestation and maintained for 7 days in rotating culture. Pyramidal cells are again organized into curved laminae, similar in many respects to the organization seen in vivo

From DeLong


Figure 1.

A: photomicrograph of leech segmental ganglion, viewed from its ventral aspect. A few of the individually recognizable cells are labeled: T, touch cells; P, pressure cells; N, cells responsive only to noxious stimuli; R, giant Retzius cells; L, longitudinal motoneurons; A, annulus erector motoneurons, Con, connectives to adjacent ganglion.

From Nicholls & Baylor . B: diagrammatic representation of the skin receptive fields of different leech ganglia, sensory cells, and anterior (A) and posterior (P) ganglionic roots. Territory innervated by ganglion 2 (7 annuli) is heavily outlined. Note partial overlap of the fields of each ganglion. •, sensillae in the central annulus of each field. From Baylor & Nicholls


Figure 2.

Profiles of individual neurons, within ganglia, revealed by Procion yellow injection. A: leech ganglion touch cell; fine synaptic terminals in the ganglionic neuropile and axonal branches entering the anterior and posterior roots (to right) and running toward the anterior and posterior connections are shown.

From van Essen . B: F3 flexor motoneuron of a crayfish. From Selverston & Kennedy


Figure 3.

Segregation of inputs onto a hippocampal pyramidal neuron (A) and a layer V cerebral cortical pyramidal cell (B). In A, the predominant synaptic inputs at each location are a) collaterals of afferent fibers from outside the hippocampus, b) Schaeffer collaterals, c) septal afferents, d) mossy fibers, e) basket cell terminals, f) collaterals from other pyramidal cells. In B, inputs are a) nonspecific thalamic and reticular formation axons, b) specific afferent radiation (geniculocalcarine radiation), c) contralateral afferents, d) axons of nearby stellate cells, e) recurrent collaterals of other pyramidal cells

From Scheibel & Scheibel


Figure 4.

Auditory nerve fibers near their points of termination in the cochlear nucleus. Each fiber ends in several different parts of the nucleus with grossly different terminal morphology. The fibers shown are branching to end in the anteroventral (top) and posteroventral regions (bottom) of the cochlear nucleus

From Ramón y Cajal


Figure 5.

Electromyograms of 4 pairs of homologous flexor (Fl.) and extensor (Ext.) muscles in a normal (N) limb and a supernumerary (T) limb receiving input predominantly from one branch of the fifth spinal nerve. Although the patterns of activity are often quite similar, in other cases the homologous muscles act totally asynchronously

From Czéh & Székely


Figure 6.

Displacement of inappropriate nerve from a cross‐innervated fish eye muscle. Experimental design is shown at top. Superior oblique muscle (S‐O) was denervated near the cord, while the inferior oblique muscle (I‐O) was removed, leaving the I‐O nerve near the denervated S‐O muscle. Degree of rotation of the eye (vertical axis) to compensate for rotation of the body (horizontal axis) is shown below. ○, unoperated left eye; •, right eye immediately after operation; Δ, right eye 2 wk later, with S‐O muscle innervated by the I‐O nerve; •, right eye 6 wk later, after S‐O nerve had regrown into muscle

From Marotte & Mark


Figure 7.

Spread of peripheral motor fields and repression of synapses in axolotl limbs. Each pair of limbs represents the hindlimbs of an experimental animal in which the right limb shows normal innervation by spinal nerves 15 (lines slanting down to right), 16 (dots), and 17 (lines slanting down to left). The dark area in the right limb, top, represents innervation by both spinal nerves 15 and 16. The motor fields differ slightly from animal to animal but are normally quite symmetrical in a given individual. In the animal shown at top, nerve 16 in the left limb was denervated 7 days before testing. Already the fields of nerves 15 and 17 had expanded near the base of the limb, and there were patches of innervated fibers in the midst of still denervated fibers further distally. After 2–3 wk, the entire limb is innervated by nerves 15 and 17. After 1–2 months, however, nerve 16 regrows into the muscle and reasserts control of its original territory. If, in such an animal, nerve 16 is again sectioned and the motor fields tested only 3 days later (below), all the territory of nerve 16 is well innervated by terminals of nerves 15 and 17

From Cass et al.


Figure 8.

The frog retinotectal projection, as determined by morphological and electrophysiological investigations

From Jacobson , reprinted by permission of Holt, Rinehart and Winston, Inc


Figure 9.

Regrowth pattern of goldfish optic nerve fibers following partial ablation of the retina and section of the optic nerve. M and L, medial and lateral bundles, respectively, entering tectum; A, P, D, and V, anterior, posterior, dorsal, and ventral poles, respectively, of retina

From Attardi & Sperry


Figure 10.

Projection patterns of optic nerve fibers in intact goldfish (A) and after regeneration following partial tectal ablation. In all cases, a microelectrode was moved from point to point on the surface of the tectum and the locations of receptive fields in the contralateral retina determined. Note that, as in Fig. , the nasal‐temporal retinal axis is mapped on the rostral‐caudal axis of the tectum, the superior‐inferior retinal axis in the medial‐lateral dimension of the tectum. In B, the retina shows a compressed projection onto the half‐tectum remaining after ablation. In C, part of the projection is compressed in each axis, part is normal

From Yoon


Figure 11.

Parallel and overlapping retinotectal projection from compound eyes. At top the normal projection is shown, with nasal retina indicated by solid lines, temporal retina by broken lines. In the compound eyes, the projection from each half‐retina is expanded to fill the whole tectum, and the duplicated half‐retina projects to the tectum in a way appropriate to its original location but not to its final location in the eye

From Gaze


Figure 12.

Geniculocortical projections in normal and Siamese cats. In the latter, there is abnormal contralateral input to the geniculate (hatched area), and the resultant output to the visual cortex, representing about 20° of central retinal visual field that would normally go to the opposite side of the brain, now projects to both areas 17 and 18, displacing the normal inputs. At the border between areas 17 and 18, the projection now starts at −20°, rather than at 0°, and progresses through the midline (black area) and then across the part of the retina normally supplying it. The unshaded area on either side of the abnormal projection indicates regions where binocularity of input to cortical cells is lost

From Hubel & Wiesel


Figure 13.

Inferred organization of the visual cortex of a macaque monkey. In one dimension, alternating ocular dominance columns receive input from different layers of the lateral geniculate and are driven by closely corresponding points on the 2 retinas. Perpendicular to the ocular dominance columns are a larger number of orientation‐selective columns. Lateral interaction between ocular dominance columns at layers superficial and deep to layer IV account for the predominance of binocular driving at these other layers. c, contralateral; i, ipsilateral

From Hubel & Wiesel


Figure 14.

A: critical period for the establishment of binocular driving of cortical cells. Each histogram represents the number of cells studied that showed different degrees of ocular dominance ranging from total contralateral dominance (group 1) to total ipsilateral dominance (group 7). Group 2 shows marked contralateral dominance and group 3 slight contralateral dominance; in group 4 both eyes are equally effective. Histogram i was obtained from a 3–4‐wk‐old kitten with normal visual experience; the pattern would be essentially the same if the kitten had had no visual experience. Histogram ii was derived from a kitten with the contralateral eyelid sutured closed between days 23 and 29; the lack of patterned input from that eye, during that period, resulted in total loss of effectiveness of the inputs from that eye. In histogram iii, contralateral blindfolding between approximately days 65 and 100 was much less effective in reducing contralateral driving; the effect of monocular deprivation was essentially gone with suturing after the third or fourth month (histogram iv).

From Hubel & Wiesel .] B: comparable effect of strabismus during the critical period. Experimental kittens (histogram B) had their right medial rectus muscle cut before their eyes opened, so that the 2 eyes each had visual experience but no longer fixated simultaneously on the same points in space. Animals so treated, after 3–12 mo, showed a severe loss of binocular driving of cortical neurons. Histogram B shows the results for all cells studied, compared with the dominance pattern of cells in the control animals (histogram A). [From Hubel & Wiesel


Figure 15.

Experimental scheme used to test competition between lateral geniculate cells in maintaining functional cortical connections. The left eye was sutured closed, causing visual deprivation in lamina A (the top layer) of the contralateral lateral geniculate nucleus (LGN). When the right eye is intact, this results in cell shrinkage in segments 2–4 (shaded area), which overlap in cortical projection with output from layer A1 (below). Segment 1, which is equally deprived but does not overlap in its projection, shows less or no atrophy. To test whether competitive interaction at the level of the cortex is involved, area 3 of the right retina was destroyed, eliminating input to segment 3 of layer A1. In this case, there was atrophy of the cells in segment 3 of layer A1, and reduced atrophy in segment 3 of layer A

From Guillery


Figure 16.

Experimental design and results showing plasticity of connectivity during the critical period in kittens. Kittens, wearing a ruff to prevent vision of themselves, were placed in a plastic tube and exposed only to vertical stripes (as shown) or only to horizontal stripes for several hours each day. This was their only visual experience. Shown below are the orientation specificities of all the cortical neurons studied in cats so treated. In the horizontally experienced cat (left), all cells showed a preference for horizontally oriented stimuli; all cells tested in the vertically experienced cat (right) preferred vertically oriented stimuli. Control animals show approximately equal numbers of cells preferring all orientations

From Blakemore & Cooper


Figure 17.

Number of apical dendritic spines on layer V pyramidal cortical cells in visual cortex of normal and visually deprived mice. A shows the increase in number of spines per 100‐μm segment of apical dendrite (see inset C) in mice raised with normal visual experience, in the dark, and for 20 days in the dark followed by exposure to normal lighting. The derivative of each curve is shown in B, and the numbers of experimental animals used for each point is indicated in the area between A and B. Total light deprivation caused marked retardation of synaptic spine development, while exposure to light after 20 days led to rapid recovery to the normal numbers

From Valverde


Figure 18.

Increase in number of synapses (S) by a single nerve terminal on 2 or more dendritic spines per 100 single synaptic contacts (multiple synaptic index) as a function of time after incomplete lesion of the fimbrial input to hippocampal neurons. Within 2 to 3 days after the lesion, there is a large peak in the number of degenerating synapses, followed by a gradual disappearance of degenerating terminals over a period of approximately 30 days. During these 30 days, there is a striking increase in the number of synapses by one nerve terminal on 2 or more spines. The proposed explanation for this phenomenon is that nerve fibers that remain following the lesion sprout collaterals that innervate nearby vacated spines (see inset). S, dendritic spine; D, degenerating terminal; N, normal terminal

From Raisman & Field


Figure 19.

Glial guidance of migrating neurons. Temporal and spatial reconstruction of the developing cerebellar cortex showing different stages in the migration of granule cells (D) along the Bergmann glial fiber (BGF) processes of Golgi epithelial cells (GEC), from the surface of the cerebellum through the parallel fibers (PF) and past the stellate cells (S) and Purkinje cells (PC) to their eventual location. The orientation of the various planes is indicated by the geometric figure at lower left: transverse (I) and longitudinal (II) to the folium and parallel to the pial surface (III). Diameters of cellular elements are exaggerated for purposes of illustration. MF, mossy fiber; CF, climbing fiber; SD, stellate cell dendrite; EG, external granular cell layer; M, molecular layer; P, Purkinje cell layer; G, granular layer

From Rakic & Sidman


Figure 20.

Patterned reaggregation of dissociated hippocampal cells. A: section through intact mouse hippocampus at 19 days gestation. The prominent curved lamina of pyramidal cells is conspicuous, as is the compact dentate gyrus at bottom center. B: an aggregate of hippocampal cells dissociated at 18.5 days gestation and maintained for 7 days in rotating culture. Pyramidal cells are again organized into curved laminae, similar in many respects to the organization seen in vivo

From DeLong
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Alan D. Grinnell. Specificity of Neurons and their Interconnections. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 803-853. First published in print 1977. doi: 10.1002/cphy.cp010122