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Are central pattern generators understandable?

  • Allen I. Selverston (a1)

Most rhythmic behaviors are produced by a specialized ensemble of neurons found in the central nervous system. These central pattern generators (CPGs) have become a cornerstone of neuronal circuit analysis. Studying simple invertebrate nervous systems may reveal the interactions of the neurons involved in the production of rhythmic motor output. There has recently been progress in this area, but due to certain intrinsic features of CPGs it is unlikely that present techniques will ever yield a complete understanding of any but the simplest of them. The chief impediment seems to be our inability to identify and characterize the total interneuronal pool making up a CPG. In addition, our general analytic strategy relies on a descriptive, reductionist approach, with no analytical constructs beyond phenomenological modeling. Detailed descriptive data are usually not of sufficient depth for specific model testing, giving rise instead to ad hoc explanations of mechanisms which usually turn out to be incorrect. Because they make too many assumptions, modeling studies have not added much to our understanding of CPCs; this is due not so much to inadequate simulations as to the poor quality and incomplete nature of the data provided by experimentalists.

A basic strategy that would provide sufficient information for neural modeling would include: (1) identifying and characterizing each element in the CPG network; (2) specifying the synaptic connectivity between the elements; and (3) analyzing nonlinear synaptic properties and interactions by means of the connectivity matrix. Limitations based on our present technical capabilities are also discussed.

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B. O. Alving (1968) Spontaneous activity in isolated somata of Aplysia pacemaker neurons. Journal of General Physiology 51:2945. [AIS]

P. Andersen & J. C. Eccles (1962) Inhibitory phasing of neuronal discharge. Nature (London) 196:645–47. [GS]

P. A. Anninos , B. Beek , T. J. Csermely , E. Harth & G. Pertile (1970) Dynamics of neural structures. Journal of Theoretical Biology 26:121–48. [EH]

J. L. Ayers & W. J. Davis (1977) Neuronal control of locomotion in the lobster Homarus americanus. I. Motor programs for forward and backward walking. Journal of Comparative Physiology 115:124. [JA]

J. Ayers Jr & A. I. Selverston (1979) Monosynaptic entrainment of an endogenous pacemaker network: a cellular mechanism for von Holst's magnet effect. Journal of Comparative Physiology 129:517. [HMP]

J. L. Barker , M. S. Ifshin & H. Gainer (1975) Studies on bursting pacemaker potential activity in molluscan neurons. III. Effects of hormones. Brain Research 84:501–3. [AIS]

J. L. Barker & H. Gainer (1974) Peptide regulation of bursting pacemaker activity in a molluscan neurosecretory cell. Science 184:1371–73. [AIS]

S. F. Basinger , W. C. Gordon & D. M. K. Lam (1979) Differential labelling of retinal neurones by 3H-2-deoxyglucose. Nature 280:682–84. [SCR]

U. Bässler (1977) Sensory control of leg movement in the stick insect, Carausius morosus. Biological Cybernetics 25:6172. [GW]

D. Bentley & M. Konishi (1978) Neural control of behavior. In: Annual Review of Neuroscience, vol. 1, ed. W. M. Cowan 2, W. Hall , and E. R. Kandel , pp. 3559. [HMP]

M. S. Berry & V. W. Pentreath (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Research 105:120. [AIS]

N. Bohr (1933) Light and life. Nature 131:421–57. [CML]

C. W. Bradley , C. von Euler , I. Marttila & B. Roos (1975) A model of the central and reflex inhibition of inspiration in the cat. Biological Cybernetics 19:105–16. (SG)

K. Brändle & G. Székely (1973) The control of alternating coordination of limb pairs in the newt (Triturus vulgaris). Brain, Behavior and Evolution 8:366–85. [GS]

T. G. Brown (1911) The intrinsic factors in the act of progression in the mammal. Proceedings of the Royal Society of Britain 84:308–19. [AIS]

T. G. Brown (1914) On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. Journal of Physiology (London) 48:1846. [AIS]

M. Burrows (1979) Synaptic potentials effect the release of transmitter from locust nonspiking interneurons. Science 204:8183. [TJW]

M. Burrows (1980) The control of sets of motoneurons by local interneurons in the locust. Journal of Physiology 298:213–33. [FD.AIS]

J. H. Byrne & J. Koester (1978) Respiratory pumping: neuronal control of a centrally commanded behavior in Aplysia. Brain Research 143:87105. [HMP]

R. L. Calabrese (1977) The neural control of alternate heartbeat coordination states in the leech, Hirudo medidnalis. Journal of Comparative Physiology 122:111–43. [RLC]

C. Camp & H. M. Pinsker (1979) Computer separation of unitary spikes from whole-nerve recordings. Brain Research 169:455–79. [HMP]

G. A. Carpenter (1979) Bursting phenomena in excitable membranes. SIAM Journal of Applied Mathematics 36:334–72. [AHC]

L. B. Cohen , B. M. Salzberg & A. Grinvald (1978) Optical methods for monitoring neuron activity. Annual Review of Neuroscience 1:171–82. [AIS, GLG, HMP]

W. J. Davis (1976) Organizational concepts in the central motor networks of invertebrates. In: Neural Control of Locomotion, ed. R. M. Herman , S. Grillner , P. S. G. Stein , and D. G. Stuart , pp. 265–92. New York: Plenum Press. [MM, AIS]

F. Delcomyn (1976) An approach to the study of neural activity during behaviour in insects. Journal of Insect Physiology 22:1223–27. [FD]

F. Delcomyn (1977) Corollary discharge to cockroach giant interneurones. Nature (London) 269:160–62. [FD]

F. Delcomyn (1980) Neural basis of rhythmic behavior in animals. Science (in press). [RG]

F. Delcomyn & D. Daley (1979) Central excitation of cockroach giant interneurons during walking. Journal of Comparative Physiology 130:3948. [FD]

D. A. Dorsett , A. O. D. Willows & G. Hoyle (1969) Centrally generated nerve impulse sequences determining swimming behaviour in Tritonia. Nature 224:711–12. [GH]

D. A. Dorsett , A. O. D. Willows & G. Hoyle (1973) The neuronal basis of behavior in Tritonia. IV. The central origin of a fixed action pattern demonstrated in the isolated brain. Journal of Neurobiology. 4:287300 [GH]

M. D. Eggar & R. S. Wyman (1969) A reappraisal of reflex stepping in the cat. Journal of Physiology 202:501–16. [AIS]

J. C. Fentress (1977) The tonic hypothesis and the patterning of behavior. New York Academy of Sciences 290:370–95. [JCF]

W. O. Friesen , M. Poon & G. S. Stent (1976) An oscillatory neuronal circuit generating a locomotory rhythm. Proceedings National Academy of Science, U.S.A.73:3734–38. [DKH, AIS, TJW]

W. O. Friesen & G. S. Stent (1977) Generation of a locomotory rhythm by a neural network with recurrent cyclic inhibition. Biological Cybernetics 28:2740. (RLC, WOF, JCW]

W. O. Friesen & G. S. Stent (1978) Neural circuits for generating rhythmic movements. Annual Review of Biophysics and Bioengineering 7:3761. [RG, AIS]

G. L. Gerstein & D. H. Perkel (1972) Mutual temporal relations among spike trains. Biophysical Journal 12:453–73. [GLG]

G. L. Gerstein , D. H. Perkel & K. N. Subramanian (1978) Identification of functionally related neural assemblies. Brain Research 140:4362. [GLG]

P. A. Getting (1975) Tritonia swimming: triggering of a fixed action pattern. Brain Research 96:128–33. [AIS]

P. A. Getting (1976) Afferent neurons mediating escape swimming of the marine mollusc Tritonia. Journal of Comparative Physiology 110:271–85. [AIS]

R. Gillete & W. J. Davis (1977) Role of the metacerebral giant neuron in the feeding behavior of Pleurobranchaea. Journal of Comparative Physiology 116:129–59. [SM]

R. Gillette , M. P. Kovac & W. J. Davis (1978) Command neurons in Pleurobranchaea receive synaptic feedback from the motor network they excite. Science 199:798801. [SM, AIS]

G. Gogolák , C. Stumpf , H. Petchse & J. Sterc (1968) The firing pattern of septal neurons and the form of the hippocampal theta wave. Brain Research 7:201–7. [CS]

C. S. Goodman (1978) Isogenic grasshoppers: genetic variability in the morphology of identified neurons. Journal of Comparative Neurology 182:681706. [RG]

B. Granzow & S. B. Kater (1977) Identified higher-order neurons controlling the feeding motor program of Helisoma. Neuroscience 2:1049–63. [SM]

S. Grillner (1976) Some aspects on the descending control of the spinal circuits generating locomotor movements. In: Neural Control of Locomotion, ed. R. M. Herman , S. Grillner , P. S. G. Stein , & D. G. Stuart , pp. 351–76. New York: Plenum Press. [AIS]

S. Grillner & P. Zangger (1979) On the central generation of locomotion in the low spinal cat. Experimental Brain Research 34:241–62. [SG]

A. Grinvald , B. M. Salzberg & L. B. Cohen (1977) Simultaneous recording from several neurons in an invertebrate central nervous system. Nature 268:140–42. [AIS]

L. D. Harmon (1964) Neuromimes: Action of a reciprocally inhibitory pair. Science 146:1323–25. [AIS]

E. Harth , T. J. Csermely , B. Beek & R. D. Lindsay (1970) Brain functions and neural dynamics. Journal of Theoretical Biology 26:93120. [EH]

E. Harth , N. S. Lewis & T. J. Csermely (1975) Escape of Tritonia: Dynamics of neuromuscular control mechanisms. Journal of Theoretical Biology 55:210–28. [AIS]

D. K. Hartline (1979) Pattern generation in the lobster (Panulirus) stomato-gastric ganglion. II. Pyloric network simulation. Biological Cybernetics 33:223–36. [WOF, TJW]

B. Hille (1967) The selective inhibition of delayed potassium currents in nerve by tetraethyl ammonium ion. Journal of General Physiology 50:12871302. [AIS]

E. von Holst (1935) Erregungsbildung und Erregungsleitung im Fischrückenmark. Pflügers Archiv 235:345–59. [GW]

E. von Holst (1935) Über den Prozess der zentralnervösen Koordination. Pflügers Archiv 236:149–58. [FH]

E. von Holst (1936a) Vom Dualismus der motorischen und der automatisch-rhythmischen Funktion im Rückenmark und vom Wesen des automatischen Rhythmus. Pflügers Archiv 237:356–78. [FH, GW]

E. von Holst (1936b) Versuche zur Theorie der relativen Koordination. Pflügers Archiv 237:93121. [FH]

E. von Holst (1937) Vom Wesen der Ordnung im Zentralnervensystem. Naturwissen-schaften 25:625–31, und 641–47. [FH]

E. von Holst (1939) Die relative Koordination als Phänomen und als Methode zentralnervöser Funktionsanalyse. Ergebnisse der Physiologie 42:228306. [GW]

G. Hoyle (1975) Identified neurons and the future of neuroethology. Journal of Experimental Zoology 194:5174. [GH]

J. Jalife & C. Antzelevitch (1979) Phase resetting and annihilation of pacemaker activity in cardiac tissues. Science 206:695–97. [HMP]

E. Jankowska , M. G. M. Jukes , S. Lund & A. Lundberg (1967) The effect of DOPA on the spinal cord. V. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiological Scandinavica 70:369–88. [SG]

E. Jankowska , M. G. M. Jukes , S. Lund & A. Lundberg (1967) The effect of DOPA on the spinal cord. VI. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiologica Scandinavica 70:389402. [AIS]

S. B. Kater (1974) Feeding in Helisoma trivolvis: The morphological and physiological basis of a fixed action pattern. American Zoologist 14:1017–36. [AIS]

C. R. S. Kaneko , M. Merickel & S. B. Kater (1978) Centrally programmed feeding in Helisoma: identification and characteristics of an electrically coupled premotor neuron network. Brain Research 146:121. [CRSK, MM]

C. Kennedy , M. H. Des Rosiers , J. Jehle , W. Reivich , F. Sharpe & L. Sokoloff (1975) Mapping of functional neural pathways by autoradiographic survey of local metabolic rate with [14C]deoxyglucose. Science 187:850–53. [AIS]

U. Kling & G. Székely (1968) Simulation of rhythmic nervous activities. I. Function of networks with cyclic inhibitions. Kybernetik 5:89103. [GS]

W. B. Kristan (1974) Neural control of swimming in the leech. American Zoologist 14:9911001. [AIS]

E. R. Macagno , V. Lopresti & C. Levinthal (1973) Structure and development of neuronal connections in isogenic organisms: variations and similarities in the optic system of Daphnia magna. Proceedings of the National Academy of Sciences 70:5761. [EH]

W. S. McCulloch & W. Pitts (1943) A logical calculus for ideas immanent in nervous activity. Bulletin of Mathematical Biophysics 5:115–33. [GH]

W. McDougall (1903) The nature of inhibitory processes within the nervous system. Brain 26:153–91. [WOF]

D. M. Maynard & A. I. Selverston (1975) Organization of the stomatogastric ganglion of the spiny lobster. IV. The pyloric system. Journal of Comparative Physiology 100:161–82. [AIS]

D. M. Maynard & K. D. Walton (1975) Effects of maintained depolarization of presynaptic neurons on inhibitory transmission in lobster neuropil. Journal of Comparative Physiology 97:215–43. [TJW]

M. Mendelson (1971) Oscillator neurons in crustacean ganglia. Science 171:1170–73. [AIS]

M. Merickel & R. Gray (1980) Investigation of burst generation by the electrically coupled cyberchron network in the snail Helisoma using a single-electrode voltage clamp. Journal of Neurobiology 11:73102. [CRSK, MM, SM]

J. P. Miller & A. Selverston (1979a) Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 206:702–4. [SG, AIS]

S. J. Mitchell & J. B. Ranck Jr (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Research 189:4966. [GS]

B. Möhl & W. Nachtigall (1978) Proprioceptive input on the locust flight motor revealed by muscle stimulation. Journal of Comparative Physiology 128:5765. [GW]

J. Morris & D. M. Maynard (1970) Recordings from the stomatogastric nervous system in intact lobsters. Comparative Biochemistry and Physiology 33:969–74. [HMP]

B. Mulloney & A. I. Selverston (1974) Organization of the stomatogastric ganglion of the spiny lobster. I. Neurons driving the lateral teeth. Journal of Comparative Physiology 91:132. [AIS]

K. G. Pearson & C. S. Goodman (1979) Correlation of variability in structure with variability in synaptic connections of an identified interneuron in locusts. Journal of Comparative Neurology 184:141–66. [RG]

D. H. Perkel , G. L. Gerstein & G. P. Moore (1967) Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophysical Journal 7:419–40. [GLG]

D. H. Perkel , G. L. Gerstein , M. S. Smith & W. G. Tatton (1975) Nerve impulse patterns. Brain Research 100:271–96. [GLG]

D. H. Perkel & B. Mulloney (1974) Motor pattern production in reciprocally inhibitory neurons exhibiting postinhibitory rebound. Science 185:181–83. [RG, AIS, TJW]

E. L. Peterson & M. D. R. Jones (1979) Do circadian oscillators ever stop in constant light? Nature 280:677–79. [HMP]

J. A. Raper (1979) Nonimpulse-mediated synaptic transmission during the generation of a cyclic motor program. Science 205:304–6. [RG, TJW]

K. D. Roeder (1948) Organization of the ascending giant fiber system in the cockroach (Periplaneta americana L.). Journal of Experimental Zoology 108:243–62. [FD]

D. F. Russell & D. K. Hartline (1978) Bursting neural networks: a reexamination. Science 200:453–56. [AHC, RLC, RG, MM, SCR, TJW]

F. O. Schmitt , P. Dev & B. H. Smith (1976) Electronic processing of information by brain cells. Science 193:114–20. [SG]

A. I. Selverston (1976) Neuronal mechanisms for rhythmic motor pattern generation in a simple system. In: Neural Control of Locomotion, ed. R. M. Herman , S. Grillner , P. S. G. Stein , & D. G. Stuart , pp. 377400. New York: Plenum Press. [AIS]

A. I. Selverston & B. Mulloney (1974) Organization of the stomatogastric ganglion of the spiny lobster. II. Neurons driving the medial tooth. Journal of Comparative Physiology 91:3351. [TJW]

M. V. S. Siegler & M. Burrows (1980) Non-spiking interneurones and local circuits. Trends in Neurosciences 3:7377. [SC]

M. E. Spira & M. V. L. Bennett (1972) Synaptic control of electrotonic coupling between neurons. Brain Research 37:294300. [AIS]

M. E. Spira , D. C. Spray & M. V. L. Bennett (1976) Electrotonic coupling: Effective sign reversal by inhibitory neurons. Science 194:1065–67. [AIS]

P. S. G. Stein (1976) Mechanisms of interlimb phase control. In: Neural Control of Locomotion, ed. R. M. Herman , S. Grillner , P. S. G. Stein , & D. G. Stuart , pp. 465–88. New York: Plenum Press. [AIS]

A. J. Susswein & I. Kupfermann (1976) The stimulus control of biting in Aplysia. Journal of Comparative Physiology 108:7596. [SCR]

G. Székely & G. Czéh (1976) Organization of locomotion. In: Frog Neurobiology, ed. R. Llinás and W. Precht , pp. 765–92. Berlin and Heidelberg: Springer-Verlag. [GS]

W. J. Thompson & G. S. Stent (1976) Neuronal control of heartbeat in the medicinal leech, I. Generation of the vascular constriction rhythm by heart motor neurons. Journal of Comparative Physiology 111:261–79. [RLC. AIS]

W. J. Thompson & G. S. Stent (1976b) Neuronal control of heartbeat in the medicinal leech. II. Intersegmental coordination of heart motor neuron activity by heart interneurons. Journal of Comparative Physiology 111:281307. [RLC]

W. J. Thompson & G. S. Stent (1976c) Neuronal control of heartbeat in the medicinal leech. III. Synaptic relations of the heart interneurons. Journal of Comparative Physiology 111:309–33. [RLC]

S. N. Treistman (1979) Duplication of a spontaneously active neuron in Aplysia. Journal of Neurobiology 10:325–30. [RG]

S. N. Treistman & J. H. Schwartz (1976) Functional constancy in Aplysia nervous systems with anomalously duplicated identified neurons. Brain Research 109:607–14.

J. F. Viebert , F. Bertrand , M. Denavit-Saubié , & A. Hugelin (1976) Three dimensional representation of bulbo-pontine respiratory networks architecture from unit density maps. Brain Research 114:227–44. [GS]

H. S. Warshaw & D. K. Hartline (1976) Simulation of network activity in stomatogastric ganglion of the spiny lobster, Panulirus. Brain Research 110:259–72. [TJW]

K. R. Weiss & I. Kupfermann (1976) Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs. Brain Research 117:3349. [SM]

G. Wendler (1974) The influence of proprioceptive feedback on locust flight co-ordination. Journal of Comparative Physiology 88:173200. [HMP, GW]

J. Westin , J. J. Langberg & J. M. Camhi (1977) Responses of giant interneurons of the cockroach Periplaneta americana to wind puffs of different direction and velocities. Journal of Comparative Physiology 121:307–24. [FD]

A. O. D. Willows (1976) Trigger neurons in the mollusk Tritonia. In: Neural Control of Locomotion, ed. R. M. Herman , S. Grillner , P. S. G. Stein , & D. G. Stuart , pp. 327–50. New York: Plenum Press. [AIS]

A. O. D. Willows , D. A. Dorsett & G. Hoyle (1973) The neuronal basis of behavior in Tritonia. III. Neuronal mechanism of a fixed action pattern. Journal of Neurobiology 4:255–85. [AIS]

D. M. Wilson & I. Waldron (1968) Models for the generation of the motor output pattern in the flying locust. Proceedings of Institute of Electrical & Electronics Engineers 56:1058–64. [AIS]

A. Winfree (1977) Phase control of neural pacemakers. Science 197:761–63. [HMP]

R. Wong & E. Harth (1973) Stationary states and transients in neural populations. Journal of Theoretical Biology 40:77106. [EH]

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