click for enlargement of this Mark Meyer painting

THE CEREBRAL CODE Thinking a Thought in the Mosaics of the Mind Available from MIT Press and amazon.com. copyright 1996 by William H. Calvin

Notes Because good medical libraries are few and far between, I have attempted to cite the most widely available articles and books (though I often have to cite specialty journals instead). Short-form citations such as Dennett (1995) either refer to a book in my Recommended Reading list or to a nearby full-length citation. Prologue page numbers refer to the MIT Press edition 1 Stephen Jay Gould, Ontogeny and Phylogeny (Harvard University Press 1977). 1 See the last chapter of Jean Piaget, Le langage et la pensee chez l'enfant (Neuchatel 1923). 3 This use of code subsumes the more common uses of neural code, e.g., those referring to firing rate, spike timing, etc., all of which are derivative of the 1950's auditory place versus frequency code debates. Code often just means representation or mapping. For some modern discussion, see Terrence J. Sejnowski, "Time for a new neural code?" Nature 376:21-22 (6 July 1995); John J. Hopfield, "Pattern recognition computation using action potential timing for stimulus representation," Nature 376:33-36 (6 July 1995); Sam A. Deadwyler and Robert E. Hampson, "Ensemble activity and behavior: what's the code?" Science 270:1316-1318 (24 November 1995); A. P. Georgopoulos, A. Ashe, N. Smyrnis, M. Taira, "The motor cortex and the coding of force," Science 256: 1692-1695 (1992). 4 Kenneth J. W. Craik, The Nature of Explanation (Cambridge University Press 1943), p. 61. 4 Dennett (1995). 4 William H. Calvin, "The brain as a Darwin Machine." Nature 330:33-34 (5 November 1987). 4 William James's development of his darwinian theory of mind, see pp. 433ff of Robert J. Richards, Darwin and the Emergence of Evolutionary Theories of Mind and Behavior (University of Chicago Press 1987). The modern chapter of mental darwinism starts in 1965 with Dan Dennett's D. Phil. thesis, published as Content and Consciousness (Routledge and Kegan Paul 1969). 4 Other examples of darwinian processes include so-called "genetic algorithms" in computer science and molecular biology techniques seen in the RNA evolution experiments. See John H. Holland, "Genetic algorithms," Scientific American 267(1):66-72 (July 1992). Gerald F. Joyce, "Directed molecular evolution," Scientific American 267(6):90-97 (December 1992). 5 Ludwig Wittgenstein, Philosophical Investigations (Basil Blackwell 1953). 5 J. Allan Hobson, The Dreaming Brain (Basic Books 1988). 5 Charles Darwin, On the Origin of Species (1859). 6 "...most "darwinian" discussions...." See articles in Sporns and Tonini (1994). 6 The background is in William H. Calvin, " Islands in the mind: dynamic subdivisions of association cortex and the emergence of a Darwin Machine," Seminars in the Neurosciences 3(5):423-433 (1991). William H. Calvin, ``The emergence of intelligence,'' Scientific American 271(4):100-107 (October 1994; also appears in the Scientific American book Life in the Universe, 1995 -- N.B., the hexagons figure is an editorial error; simply ignore it or see the web page for the unaltered version. 6 This book-length consideration of the issues was delayed by several other books in progress, though I did manage some brief treatments, e.g., in the last chapter of Conversations with Neil's Brain: The Neural Nature of Thought and Language and in the latter half of my Scientific American article. Chapter 7 of How Brains Think summarizes my neocortical Darwin Machine scheme but The Cerebral Code is its first complete description. 7 Charles Ives, see p. 366 of Joseph Machlis, The Enjoyment of Music, "5th ed. shorter" (W. W. Norton 1984). 8 Mac Wells illustrated my archaeoastronomy book, How the Shaman Stole the Moon (Bantam 1991). 8 Simulations were half of my Ph.D. thesis, a means of seeing if observed noise could account for the actual stochastic interspike interval variability of cat spinal motor neurons. I have been skeptical of free-parameter curve-fitting that is hidden from view even of the simulation's proprietor ever since. See W. H. Calvin and C. F. Stevens, "Synaptic noise and other sources of randomness in motoneuron interspike intervals," Journal of Neurophysiology 31:574-587 (1968). 9 Ernst Mayr, "Population thinking and neuronal selection: metaphors or concepts?" In Selectionism and the Brain, edited by Olaf Sporns and Giulio Tonini (Academic Press 1994), pp.27-34 at p.29. 9 Niels K. Jerne, "Antibodies and learning: Selection versus instruction," in The Neurosciences: A Study Program, edited by G. C. Quarton, T. Melnechuk, & F. O. Schmitt (Rockefeller University Press 1967), pp. 200-205 at p. 204.

Chapter 1. The Representation Problem and the Copying Solution 11 Antonio R. Damasio, Descartes' Error (Putnam 1995), p.12. 11 Those aware of the philosophical battles over the word representation should realize that I'm always using it in the sense of a cerebral code, not an external symbol or sign. For a similar neurophysiologically-based perspective that bypasses unnecessary hangups, see Freeman (1995), pp. 106-108. 11 Christmas dinner quip: Freeman (1995), p.55. 13 Taste coding: Robert P. Erickson, "On the neural bases of behavior," American Scientist 72:233-241 (May-June 1984). An endnote in my The Cerebral Symphony, at p. 359, discusses its application to orientation-sensitive neurons of visual cortex with eighteen types of elementary templates. 13 Irving Kupferman, Kenneth R. Weiss, "The command neuron concept," Behavioral and Brain Science 1(1):3-39 (1978). 13 Schemas, see Johnson (1987). 13 Donald O. Hebb, The Organization of Behavior (Wiley 1949). And see Peter M. Milner, "The mind and Donald O. Hebb," Scientific American 268(1):124-129 (January 1993). 13 It is just as important that the other lights are off: indeed, it is well to occasionally recall that vertebrate photoreceptors have their maximum rate of neurotransmitter discharge in darkness; what the image of a star against the night star does is to create a local hole in a sea of photoreceptor activity. That this isn't necessarily seen at later stages of the visual pathway only testifies to the amount of spatial and temporal differencing that occurs in other layers of the retina. 14 Automata, see William Poundstone, The Recursive Universe (Morrow 1985). 15 Hebb (1949), p. 62. 16 Representations don't have to be codes, so long as they remain local. The withdrawal reflex is wired up so that various combinations of threatening stimuli get an appropriate set of motor neurons up and running. Yes, there's a representation of threat, but not necessarily a code in the sense of a cell-assembly of stereotyped pattern. 16 Donald O. Hebb, Essay on Mind (Erlbaum 1980), epigram at p.1, history at p.81. 17 Predicting movements, see Georgopoulos et al (1992). 17 Patricia S. Goldman-Rakic, "Working memory and the mind," Scientific American 267(3):73-79 (September 1992). 17 Moshe Abeles, Corticotonics: Neural Circuits of the Cerebral Cortex (Cambridge University Press 1991). E. Vaadia, I. Haalman, M. Abeles, H. Bergman, Y. Prut, H. Slovin, A. Aertsen, "Dynamics of neuronal interactions in monkey cortex in relation to behaviourial events," Nature 373:515-518 (9 February 1995). 18 Erwin Schrödinger, What is Life? (Cambridge University Press 1944). 22 Gerald F. Joyce, "Directed molecular evolution," Scientific American 267(6):90-97 (December 1992). 22 Holland (1992). 23 There is potentially an enormous difference, in some species, between what's conceived and what survives in utero long enough to be born. In humans, only about one in five conceptions results in a term birth, suggesting that environmental factors could play a large role in biasing the characteristics of a human population. 24 "Lean mean machine...." Calvin (1996). 24 A. M. Lister, "Rapid dwarfing of red deer on Jersey in the last interglacial," Nature 342:539-542 (30 November 1989). 25 Darwin (1859) writes in Chapter III: The number of humble-bees in any district depends in a great measure upon the number of field-mice, which destroy their combs and nests; and Col. Newman, who has long attended to the habits of humble-bees, believes that "more than two-thirds of them are thus destroyed all over England." Now the number of mice is largely dependent, as every one knows, on the number of cats; and Col. Newman says, "Near villages and small towns I have found the nests of humble-bees more numerous than elsewhere, which I attribute to the number of cats that destroy the mice." Hence it is quite credible that the presence of a feline animal in large numbers in a district might determine, through the intervention first of mice and then of bees, the frequency of certain flowers in that district! 25 Jonathan Weiner, The Beak of the Finch (Knopf 1994). 25 avoir l'esprit de l'escalier is from Howard Rheingold, They Have a Word for It (Tarcher 1987). 25 A female that selects a mate on the basis of quick mental performance in a male thereby augments the quickness of both her sons and (unless the gene is on the Y chromosome) daughters.

Chapter 2. Cloning in Cerebral Cortex For the local circuits of cerebral cortex, see the special issue of the journal Cerebral Cortex 3 (September/October 1993) edited by Kathleen S. Rockland. An introduction to the iterated architecture aspects is William H. Calvin, ""Cortical Columns, Modules, and Hebbian Cell Assemblies," in Handbook of Brain Theory and Neural Networks, M. A. Arbib, ed. (MIT Press 1995), pp. 269-272. Primary visual cortex is the best-studied area: Jennifer S. Lund, "Anatomical organization of macaque monkey striate visual cortex," Annual Reviews of Neuroscience 11:253-288 (1988). 27 Richard Dawkins, The Selfish Gene (Oxford University Press 1976). 28 Von Békésy's lateral inhibition experiments are recounted in Floyd Ratliff's Mach Bands: Quantitative Studies on Neural Networks in the Retina (Holden-Day, San Francisco 1965). 28 C. Stephanis, Herbert Jasper, "Recurrent collateral inhibition in pyramidal tract neurons," Journal of Neurophysiology 27:855-877 (1964). 28 R. J. Douglas, C. Koch, M. Mahowald, K. A. Martin, H. H. Suarez, "Recurrent excitation in neocortical circuits," Science 269:981-985 (18 August 1995). 31 It's not that the axons lack synapses in the "gaps" but that they have many-branched terminal trees clustering around the metric distance. See figure 3 of Barbara A. McGuire, Charles D. Gilbert, Patricia K. Rivlin, Torsten N. Wiesel, "Targets of horizontal connections in macaque primary visual cortex," Journal of Comparative Neurology 305:370-392 (1991). Their Cell 1 is reproduced with permission in the present illustration. 31 R. A. Fisken, L. J. Garey, T. P. S. Powell, "The intrinsic, association, and commissural connections of the visual cortex," Philosophical Transactions of the Royal Society (London) 272B:487-536 (1975). 31 The lattice connectivity in the superficial layers has been seen in all mammals examined except rats; even a marsupial, the quokka, has them (J. S. Lund, Seattle lecture, 27 February 1996). 31 Greg Stuart, Bert Sakmann, "Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons," Neuron 15:1065-1076 (November 1995). 32 A. Das, Charles D. Gilbert, "Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex," Nature 375:780ff (29 June 1995). The inset illustration is a gray scale version of their color figure, as is the earlier "Mexican hat" figure. 32 Atsushi Iriki, Constantine Pavlides, Asaf Keller, Hiroshi Asanuma, "Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents," Journal of Neurophysiology 65:1435-1441 (1991). 32 Rafael Lorente de Nó, "Analysis of the activity of the chains of internuncial neurons," Journal of Neurophysiology 1:207-244 (1938). Also see his article on cerebral cortex at pp. 288-315 in the 3d edition of John F. Fulton's Physiology of the Nervous System, Oxford University Press (1949). 32 Abeles (1991). 33 David Somers and Nancy Kopell, "Rapid synchronization through fast threshold modulation," Biological Cybernetics 68:393-407 (1993). J. T. Enright, "Temporal precision in circadian systems: a reliable neuronal clock from unreliable components?" Science 209:1542-1544 (1980). 33 Hugh Smith, "Synchronous flashing of fireflies," Science 82:51 (1935). 33 Steven Strogatz, Ian Stewart, "Coupled oscillators and biological synchronization," Scientific American 269:102-109 (December 1993). 33 Wolf Singer, "Synchronization of cortical activity and its putative role in information processing and learning," Annual Review of Physiology 55:349-374 (1993). 36 "Stepping connectivity" is a more general term than lattice, used to cover the instances where axons also terminate in stripes. The gaps and clusters are thought to be tuned up prenatally, perhaps secondary to the inhibitory actions of the large basket neurons of the superficial layers, whose axonal branches spread just wide enough to cover the gaps, but not so wide as to inhibit the next axon terminal path. If intermediate axon terminals were never successful during development because of countervailing inhibition, they might have been eliminated. The basic cluster and gap pattern of the superficial pyramidal neuron might therefore be secondary to that of the large basket neuron. The axons of the large basket neurons of the other layers do not spread widely enough to match the lattice spacing (and the ones in the rat are insufficient in all layers). See Jennifer S. Lund, Takashi Yoshioka, Jonathan B. Levitt, "Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex," Cerebral Cortex 3:148-162 (March/April 1993). 37 Other organizing principles may well be at work, competing with perfect triangles. In primary visual cortex, for example, the orientation columns, color blobs, and ocular dominance factors may be pulling the clusters here and there.

Chapter 3. A Compressed Code Emerges 39 Hebb (1980), p. 88. 40 Lund et al. (1993). 41 E. Rausell, E. G. Jones, "Extent of intracortical arborization of thalamocortical axons as a determinant of representation in monkey somatic sensory cortex," Journal of Neuroscience 15:4270 (1995). X. Wang, M. M. Merzenich, K. Sameshima, W. M. Jenkins, "Remodeling of hand representation in adult cortex determined by timing of tactile stimulation," Nature 378:71-75 (2 November 1995). 41 Daniel Y. Ts'o, R. D. Frostig, E. E. Lieke, A. Grinvald, "Functional organization of primate visual cortex revealed by high resolution optical imaging," Science 249:417-420 (27 July 1990). 41 William H. Calvin, Peter C. Schwindt, "Steps in production of motoneuron spikes during rhythmic firing," Journal of Neurophysiology 35:311-325 (1972). William H. Calvin, John D. Loeser, "Doublet and burst firing patterns within the dorsal column nuclei of cat and man," Experimental Neurology 48:406-426 (1975). William H. Calvin, George W. Sypert, "Fast and slow pyramidal tract neurons: An intracellular analysis of their contrasting repetitive firing properties in the cat," Journal of Neurophysiology 39:420-434 (1976). William H. Calvin, Daniel K. Hartline, "Retrograde invasion of lobster stretch receptor somata in the control of firing rate and extra spike patterning," Journal of Neurophysiology 40:106-118 (1977). 42 A. J. Rockel, R. W. Hiorns, T. P. S. Powell, "The basic uniformity in structure of the neocortex," Brain 103:221-244 (1980). They estimate about 110 neurons in a minicolumn. 43 There is a reason for starting with color: the blobs might help to fix the orientation of the triangular arrays. 43 Binding (see Glossary), e.g., the "temporal tagging" hypothesis of Francis Crick and Christof Koch, "Some reflections on visual awareness," Cold Spring Harbor Symposiums in Quantitative Biology LV:953-962 (1990). 45 Also, let me repeat my caution (p. 36) about perfect regularity: just as the triangular array nodes might be equidistant in travel time rather than distance, so the hexagons need not be perfect in terms of equidistant corresponding points. The possibility that the terminal patches simply self-organize in development, in only roughly triangular fashion, also suggests that the mosaics could look more like Penrose tilings than hexagonal mosaics. This would be particularly likely where cortex is markedly curved, as at the top and bottom of a sulcus (any volleyball will demonstrate how a spherical surface can use hexagons intermixed with pentagons). 45 William H. Calvin, "Error-correcting codes: Coherent hexagonal copying from fuzzy neuroanatomy." World Congress on Neural Networks 1:101-104 (1993).

Chapter 4. Managing the Cerebral Commons 51 Michael A. Arbib, In Search of the Person (University of Massachusetts Press 1985), pp.52-53. 52 Barbara L. Finlay and Richard B. Darlington, "Linked regularities in the development and evolution of mammalian brains," Science 268:1578-1584 (16 June 1995). 53 Charles Darwin, On the Origin of Species (John Murray, London, 1859, p. 200) notes that "every detail of structure... may be viewed as having been of special use to some ancestral form . . . -- either directly, or indirectly through the complex laws of growth." 53 Conversion and coexistence of functions in the same structure: Darwin (1859), p.137. 53 Language cortex isn't exclusively related to language: see the first few chapters of Calvin and Ojemann (1994). 54 Cicero, De oratore. 54 Garrett Hardin, "The tragedy of the commons," Science 162:1243-1248 (1968). 56 Cartesian theater fallacy, see Daniel C. Dennett, Consciousness Explained (Little, Brown 1991). 56 For an interesting discussion of self awareness in robots, see John McCarthy's "Making Robots Conscious of their Mental States" at http://www-formal.stanford.edu/jmc/consciousness-submit/consciousness-submit.html. 58 For human motor cortex, there is nice evidence that, as one learns a serial reaction time task, the excitability of relevant regions of cortex increases, as seen by wider areas from which a standard transcranial magnetic stimulus could elicit an EMG response from relevant muscle groups. By the time that reaction time finally reaches a maintained minimum, however, the area drops. See Alvaro Pascual-Leone, Jordan Grafman, Mark Hallett, "Modulation of cortical motor output maps during development of implicit and explicit knowledge," Science 263:1287-1289 (1994). While this expansion might correspond to bigger hexagonal territories, it could also correspond to generating a variety of alternate motor programs, with the final drop corresponding to no longer needing to flounder around. 58 Mass action in the nervous system (also the title of a classic 1975 book by the neurophysiologist Walter J. Freeman) is an old theme in neurophysiology, best presented in Freeman's Societies of Brains (Erlbaum 1995). 61 Karl Popper (1979), quoted by Raphael Sassower in Cultural Collisions: Postmodern Technoscience (Routledge). 61 Donald T. Campbell, "Epistemological roles for selection theory," Evolution, Cognition, and Realism: Studies in Evolutionary Epistemology, edited by N. Rescher (Lanham, MD: University Press of America 1990), pp. 1-19 at p. 9.

Chapter 5. Resonating with your Chaotic Memories 63 Cicero (104-43 B.C.), Tusculan Disputions. Friedrich Wilhelm Nietzsche, p. 360 in W. H. Auden and L. Kronenberger, The Viking Book of Aphorisms (Viking 1962). George Santayana, p. 323 in Auden and Kronenberger (1962). 63 Finches, see Weiner (1994). 64 "Activating the EEG" in small regions of neocortex: Itzhak Fried, George Ojemann, Eberhard Fetz, "Language-related potentials specific to human language cortex," Science 212:353-356 (1981). 64 Elizabeth F. Loftus, Eyewitness Testimony (Harvard University Press 1979). See Sporns and Tonini (1994) and Calvin and Ojemann (1994, chapters 7 and 8) for a summary of the editing of preexisting connections. 66 Chaos, see Abraham et al (1990), Freeman (1995), and Stewart (1995). 66 Flutters like a butterfly: Freeman (1995), p. 63. 67 The bursting behavior that one sees in epileptic foci of cerebral cortex in between seizures is not necessarily a little seizure: W. H. Calvin, "Normal repetitive firing and its pathophysiology." In: Epilepsy: A Window to Brain Mechanisms, J. Lockard and A. A. Ward, Jr., eds. (Raven Press 1980), pp. 97-121. For an application of chaos theory to the bursting problem, see Steven J. Schiff et al, "Controlling chaos in the brain," Nature 370:615-620 (1994). For the role of synchronous input, see X. Wang, M. M. Merzenich, K. Sameshima, W. M. Jenkins, "Remodeling of hand representation in adult cortex determined by timing of tactile stimulation," Nature 378:71-75 (1995). Markus Meister, Leon Lagnado, Denis A. Baylor, "Concerted signaling by retinal ganglion cells," Science 270:1207-1210 (17 November 1995). 68 Patricia K. Kuhl, "Learning and representation in speech and language." Current Opinion in Neurobiology 4:812-822 (1994). 69 Freeman (1995), p. 67. 70 A discussion of LTP, and of activity-dependent structural changes at synapses, can be found in most neurobiology texts, such as Eric R. Kandel, James H. Schwartz, Thomas M. Jessell, Principles of Neural Science, 3d edition (Elsevier 1991). 70 Karl S. Lashley, Brain Mechanisms and Intelligence (University of Chicago Press 1929). 71 For some background on the problem of assembling the ensemble, see Wolf Singer, "Development and plasticity of cortical processing architectures," Science 270:758-764 (3 November 1995). 74 Peter A. Getting, "Emerging principles governing the operation of neural networks," Annual Reviews of Neuroscience 12:185-204 (1989). 75 NMDA channel properties, see Charles F. Stevens, "Two principles of brain organization: a challenge for artificial neural networks," in The Neurobiology of Neural Networks, edited by Daniel Gardner (MIT Press 1993), pp. 13-20 at p.18. 75 This is perhaps not the time to talk about temporal summation (see the random arrivals examples in Calvin 1980, cited later) but it should be noted that NMDA channels also contribute to a slower decay of EPSPs and thus greater summation for an additional reason. Furthermore, the calcium ion entry through an NMDA channel likely stimulates various second messenger mechanisms inside the neuron. 76 Information is just becoming available for the layer 5 pyramidal neurons from loose patch recordings on both soma and apical dendrite. Action potentials consistently following EPSPs may enhance them by 20 percent but it takes fairly large voltage changes, perhaps even calcium spikes nearby, to effectively condition the EPSPs. See Greg Stuart and Bert Sakmann, "Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons," Neuron 15:1065-1076 (1995). A. M. Brown, Peter C. Schwindt, Wayne Crill, "Different voltage dependence of transient and persistent Na+ currents is compatible with modal-gating hypothesis for sodium channels," Journal of Neurophysiology 71:2562-2565 (1994). 77 One simple theory is that there are two calcium-current thresholds in dendrites, the lower one associated with long-term depression and the higher one with long-term potentiation. See C. Hansel, A. Artola, Wolf Singer, "Ca2+ signals associated with the induction of long-term potentiation and long-term depression in pyramidal cells of the rat visual cortex," Society for Neuroscience Abstracts 711.3 (1995). 77 Cortical neurons are individually capable of firing rhythmically to sustained inputs: William H. Calvin, George W. Sypert, "Fast and slow pyramidal tract neurons: An intracellular analysis of their contrasting repetitive firing properties in the cat," Journal of Neurophysiology 39:420-434 (1976). 77 W. R. Softky, Christof Koch, "The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs," Journal of Neuroscience 13:334-50 (1993). 77 Mea culpa. I spent a fair amount of time trying to convince people that cortical neurons ought to fire rhythmically, just like motor neurons, that they were impressively analog: W. H. Calvin, "Normal repetitive firing and its pathophysiology," in Epilepsy: A Window to Brain Mechanisms (J. Lockard and A. A. Ward, Jr., eds.), Raven Press, New York, pp. 97-121 (1980). The analog aspects may, of course, still be a major factor in the dendritic amplification of synaptic inputs, even in those cases where coincidence detection seems to be the name of the game: see Coincidence Detection in the Nervous System, edited by Jennifer Altman (Human Frontier Science Program, Strasbourg 1996). 78 Lots of triangular array activity would be my favorite candidate for a region of neocortex doing something interesting, not overall levels of activity as indicated by blood flow or metabolism. Note that, in the transition from disorganized activity to sharpened-up triangular arrays, an AGC might effectively mask such more traditional indicators of neocortical "activity." More firing would occur at nodes of triangular arrays, and less would occur nearby, thanks to the AGC -- and there might be no net change in the activity spatially averaged for a blood-flow-based technique to detect. 79 Abeles (1991). 79 Peter König, Andras K. Engel, Wolf Singer, "Relation between oscillatory activity and long-range synchronization in cat visual cortex," Proceedings of the National Academy of Sciences U.S.A. 92:290-294 (1995). 79 Herbert A. Simon, The Sciences of the Artificial (MIT Press 1969), pp. 95-96.

Chapter 6. Partitioning the Playfield 81 John Z. Young, A Model of the Brain (Claredon Press 1964). His "The organization of a memory system," Proceedings of the Royal Society (London) 163B:285-320 (1965) introduces the mnemon concept in which weakened synapses serve to tune up a function. A later version is his "Learning as a process of selection," Journal of the Royal Society of Medicine 72:801-804 (1979). An important predecessor, pointed out to me by Richard Dawkins in 1998, is the paper by J. W. S. Pringle, "On the parallel between learning and evolution," Behaviour 3:174-215 (1951). 81 Richard Dawkins, "Selective neurone death as a possible memory mechanism," Nature 229:118-119 (1971). 82 Jean-Pierre Changeux, A. Danchin, "Selective stabilization of developing synapses as a mechanism for the specification of neuronal networks," Nature 264:705-712 (1976). 82 Gerald M. Edelman, "Group selection and phasic reentrant signaling: a theory of higher brain function," in The Neurosciences Fourth Study Program, edited by F. O. Schmitt and F. G. Worden, pp. 1115-1139 (MIT Press 1979). 82 Three-fold range in size of primary visual cortex among adults: Suzanne S. Stensaas, D. K. Eddington, and W. H. Dobelle, "The topography and variability of the primary visual cortex in man," Journal of Neurosurgery 40:747-755 (June 1974). 82 For a recent version of the silent synapse story, see Patrick D. Wall, "Do nerve impulses penetrate terminal arborizations? A pre-presynaptic control mechanism," Trends in Neurosciences 18:99-103 (February 1995). 82 Otto Rössler, "The chaotic hierarchy," Zeitschrift für Naturforschung 38A:788-802 (1983). 82 Gerald M. Edelman, Neural Darwinism (Basic Books 1987). William H. Calvin, "A global brain theory (a book review of Gerald Edelman's Neural Darwinism)," Science 240:1802-1803 (24 June 1988). 83 "Differential amplification of particular variants in a population," is from Edelman (1989), p. 39. 83 "[This] is a population theory," Edelman (1987), p. 31. 85 Overwriting: Loftus (1979). 85 Hippocampus does replay firing sequences during sleep: see William E. Skaggs, Bruce L. Macnaughton, "Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience," Science 271:1870-1873 (29 March 1996). 85 G. Buzháki, A. Bragin, J. J. Chrobak, Z. Nádasdy, A. Sik, M. Hsu, A. Ylinen, "Oscillatory and intermittent synchrony in the hippocampus: relevance to memory trace formation," pp. 145-172. in Temporal Coding in the Brain, edited by G. Buzháki et al (Springer 1994). 85 "Timing jitter" is also easily solved via lots of clones. The modern version of the "throwing theory" is in William H. Calvin, "The unitary hypothesis: A common neural circuitry for novel manipulations, language, plan-ahead, and throwing?" pp. 230-250 in Tools, Language, and Cognition in Human Evolution, edited by Kathleen R. Gibson and Tim Ingold (Cambridge University Press 1993). 86 Hyperacuity in sensation: William H. Calvin, "Precision timing requirements suggest wider brain connections, not more restricted ones," Behavioral and Brain Sciences 7:334 (1984). 86 Evolutionarily stable strategies (ESSs), see John Maynard Smith, The Evolution of Sex (Cambridge University Press 1978). 88 Actually, because axons may have several clusters of terminals along a run, spaced "0.5 mm" apart, gateways do not have to be open, only thin. 95 Niche quote is from Ernst Mayr, Toward a New Philosophy of Biology (Harvard University Press 1988), p. 135. In G. E. Hutchinson's definition, niche is a multidimensional resource space. 95 Borneo quote is from Mayr (1988), p. 136. 96 Potential niche space: Mayr (1988), p. 129. 96 Spreadsheet evolution is discussed in my book, The River that Flows Uphill (Sierra Club Books 1987), Day 13. 97 Evolutionarily stable strategies (ESSs) surely constitute a meta-level for the cortical competitions. Just as they explained why immediate self-interest wasn't always the name of the game for the prisoner's dilemma and the like, so ESSs will probably prove relevant to the work space competitions. Once simulation of a neocortical Darwin machine handles the simple competitions, it will be interesting to see what cooperative phenomena are like. But it lies beyond the capabilities of the present analysis, that primarily relies on the mosaics of plane geometry for explanatory power. 98 James L. Gould and Carol Grant Gould, The Animal Mind, Scientific American Library, p. 43, 1994. William James, "Great men, great thoughts, and the environment," The Atlantic Monthly 46(276):441-459 (October 1880).

Intermission Notes The chalk drawing of Charles Darwin in the 1840s is by Samuel Laurence. A color reproduction can be seen on the dust jacket of Janet Browne's Charles Darwin, Volume 1, Voyaging (1995). The original is at Darwin's country home, Down House, in the London suburbs (directions: http://WilliamCalvin.com/down_hse.html). 100 Richard Dawkins, The Extended Phenotype (Oxford 1982). 104 Roy M. Pritchard, Woodburn Heron, Donald O. Hebb, "Visual perception approached by the method of stabilized images," Canadian Journal of Psychology 14:67-77 (1960). The subject's profile, adapted from Hebb (1980, the source of the history), was redrawn from a photograph appearing in Roy M. Pritchard, "Stabilized images on the retina," Scientific American 204:72-78 (June 1961). 105 The Cheshire Cat makes its (dis)appearance in Lewis Carroll, Alice's Adventures in Wonderland (1865). 106 Sustained firing can occur from sustained inputs or from a bias in leakage currents that creates a pacemaker: see, for example, William H. Calvin, Charles F. Stevens, "Synaptic noise and other sources of randomness in motoneuron interspike intervals," Journal of Neurophysiology 31:574-587 (1968). 106 For an appreciation of Hebb by his former student and long-time colleague, Peter M. Milner (who also helped extend Hebb's cell-assembly to categories and to synchrony), see "The mind and Donald O. Hebb," Scientific American 268(1):124-129 (January 1993), and "Neural representations: some old problems revisited," Journal of Cognitive Neuroscience 8:69-77 (January 1996). 106 Hebb introduced all three major concepts for which he is now celebrated -- first the dual trace memory, then the cell-assembly, and finally the Hebbian synapse -- in just two consecutive pages (pp. 61-62) of The Organization of Behavior. In many places in the book, he is most apologetic and defensive about burdening readers with his speculations -- but Hebb, in addition to the physiological orientation he received as a student of Karl Lashley's, had an overriding conviction that theory was worth doing. This conviction was seldom shared by neuroscientists of his day, who were thoroughly impatient with theory. The situation was nothing like the healthy competition between experimentalists and theoreticians that has long existed in physics. Indeed, in the midst of my two decades of experimental work when I started doing theory part-time, theory was much maligned and there were only several full-time theorists working in neuroscience-like departments. It was only when connectionism caught everyone's attention in the mid-1980s that doing theory finally became halfway respectable among neuroscientists. And one of the things that everyone was then talking about were those retrogradely-strengthened synapses, predicted four decades earlier amidst much apology by Hebb. 107 Richard Dawkins, "Viruses of the mind," in Dennett and His Critics: Demystifying Mind, edited by Bo Dahlbom (Blackwell 1993). And see Richard Brodie, Virus of the Mind (Integral Press, Seattle 1995). 108 Permission to memorize: Franklin B. Krasne, "Extrinsic control of intrinsic neuronal plasticity: a hypothesis from work on simple systems," Brain Research 140:197-206 (1978). 111 J. Allan Hobson, The Chemistry of Conscious States (Little, Brown 1994), p.117. 111 Hebb (1980), p. 5.

Chapter 7. The Brownian Notion 113 Immanuel Kant, Critique of Pure Reason (1781; translation St. Martins Press 1965), p. A141. 114 Eleanor Rosch, see Johnson (1987). 114 Samuel Butler ("II"), quoted at p. 333 by W. H. Auden and L. Kronenberger, The Viking Book of Aphorisms (Viking 1962). 114 Bickerton (1995), pp. 51-52. 116 Simple associative memories: see Daniel L. Alkon, Memory's Voice (HarperCollins 1992). 119 Robert Holt, "The microevolutionary consequences of climate change," Trends in Evolution and Ecology 5:311-315 (1990). 120 Freeman (1995), p. 100. 121 "Future place cells," see L. F. Abbott, K. I. Blum, "Learning and generating motor sequences," Nervous Systems and Behaviour (Proceedings of the 4th International Congress of Neuroethology), p.106 (1995). 121 Efference copy dates back to E. von Holst, H. Mittelstaedt, "Das Reafferenzprinzip. Wechselwiskungen zwischen Zentralnervensystem und Peripherie," Naturwissenschaften 37:464-476 (1950). 122 J. Allan Hobson, The Chemistry of Conscious States (Little, Brown 1994), pp. 59-60. 123 "Titles to abstracts to full texts" is going to be extended, thanks to web pages where five-minute audio-visual presentations can be added. And even the half-hour canned lab tour, for the very curious, with options that demonstrate lab techniques. 123 Bruce Schneier, Applied Cryptography (Wiley 1994), p.28. 125 My musical history is taken from that of Steven R. Holtzman, Digital Mantras: The Languages of Abstract and Virtual Worlds (MIT Press 1994), pp. 18-33. 126 Particularly relevant among the cortical theories is Krishna V. Shenoy, Jeffrey Kaufman, John V. McGrann, Gordon L. Shaw, "Learning by selection in the trion model of cortical organization," Cerebral Cortex 3:239-248 (1993). 127 Hebb (1980), p. 107.

Chapter 8. Convergence Zones and a Hint of Sex 129 John Maynard Smith, The Theory of Evolution (Cambridge University Press 1993), p. 41. 130 Conduction speed in axons is a function of their diameter, the extent of their myelin wrapping, and the density of sodium channels at their nodes of Ranvier. Because sodium channels are regularly replaced, up-regulating the insertion of new channels could easily be used to increase conduction speed on a side branch. Minor hesitations at branch points also enter into consideration, though the synaptic delay is the largest hesitation -- and the most easily varied, if tuning to equalize travel time. For a theoretical analysis, see Y. Manor, Christof Koch, Idan Segev, "Effect of geometrical irregularities on propagation delay in axonal trees," Biophysical Journal 60:1424-1437 (1991). 131 I thank my colleague John W. Sunsten for the whole brain photographs; they are among the excellent collection at http://www1.biostr.washington.edu/DigitalAnatomist.html. 131 Mapping corticocorticals with strychnine: J. G. Dusser de Barenne, W. S. McCulloch, "Functional organization of the sensory cortex of the monkey," Journal of Neurophysiology 1:69-85 (1938). 131 For the columns and layers summary, see William H. Calvin, "Cortical Columns, Modules, and Hebbian Cell Assemblies," in Handbook of Brain Theory and Neural Networks, M. A. Arbib, ed. (MIT Press 1995), pp. 269-272. 131 Convergence zones, see Antonio R. Damasio, "Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition," Cognition 33:25-62 (1989). For a good example of corticocortical connectivity, see Terry W. Deacon, "Cortical connections of the inferior arcuate sulcus cortex in the macaque brain," Brain Research 573:8-26 (1992). 132 Detail of Pablo Picasso, Woman in an Armchair (1941), Musée Picasso, Paris. 134 Temporal summation of inputs, see p. 105 of Calvin and Ojemann (1994). 134 Time window of NMDA channel (at room temperature): J. M. Bekkers, C. F. Stevens, "Computational implications of NMDA receptor channels," Cold Spring Harbor Symposia on Quantitative Biology LV:131-135 (1990). 136 Another contributor to submerging the less successful is long-term depression (LTD), a reduction in synaptic strengths that occurs with conditioning stimuli that are insufficient to evoke long-term potentiation (LTP). While it is still unclear whether LTD is actually a synaptic mechanism or a reduction in dendritic amplification by calcium and sodium currents, it should have the desirable feature of reducing the size of the hot spot. 137 Gamete dimorphism, see Lynn Margulis and Dorion Sagan Origins of Sex (Yale University Press 1986) and Maynard Smith (1978). 138 Setup for sexual selection to operate: for a more complete discussion, see Cronin (1991), p.114. 140 I say "loosely analogous" because the sperm-ova dimorphism isn't due to small vs. large quantities of DNA but rather of stored energy. Still, ova do have somewhat more DNA because of the maternal-only mitochondrial mtDNA and the female's two X chromosomes. 141 Synesthesia is described in Richard E. Cytowic, The Man Who Tasted Shapes (Putnams 1993). 144 Henry J. Perkinson, Teachers Without Goals/Students Without Purposes (McGraw-Hill 1993), p. 34. Damien Broderick (1996). See http://odyssey.apana.org.au/~terminus/iq-14.html#Interview with Damien Broderick

Chapter 9. Chimes on the Quarter Hour 145 Roger Shank and Robert Abelson, Scripts, Plans, Goals and Understanding (Erlbaum 1977), p. 41. Urge to finish known sequence serving to quiet crying children: Sandra Trehub, University of Toronto, personal communication (1995). Peter Brooks, Reading for the Plot: Design and Intention in Narrative (Random House 1984), pp. 1-2. 146 Jabberwocky later appeared in Lewis Carroll, Through the Looking Glass. 147 Dennett (1995), p.139. 147 Hint: the next line is "The evil that men do lives after them. . . ." The answer is in the notes for the last chapter. 150 Gordon H. Bower and Daniel G. Morrow, "Mental models in narrative comprehension," Science 247:44-48 (1990). 151 J. Hore, S. Watts, J. Martin, B. Miller. "Timing of finger opening and ball release in fast and accurate overarm throws," Experimental Brain Research 103: 277-286 (1995). J. Hore, S. Watts, D. Tweed, "Arm position constraints when throwing in three dimensions," Journal of Neurophysiology 72: 1171-1180 (1994). 151 William H. Calvin, Charles F. Stevens, "Synaptic noise as a source of variability in the interval between action potentials," Science 155:842-844 (1967). 152 William H. Calvin, "A stone's throw and its launch window: timing precision and its implications for language and hominid brains," Journal of Theoretical Biology 104:121-135 (1983). 152 William H. Calvin, George W. Sypert, "Fast and slow pyramidal tract neurons: An intracellular analysis of their contrasting repetitive firing properties in the cat," Journal of Neurophysiology 39:420-434 (1976). 153 John R. Clay, Robert DeHaan, "Fluctuations in interbeat interval in rhythmic heart-cell clusters," Biophysical Journal 28:377-389 (1979). 153 J. T. Enright, "Temporal precision in circadian systems: a reliable neuronal clock from unreliable components?" Science 209:1542-1544 (1980). 154 Brian Eno, radio interview on Fresh Air (1990) and personal communication (1995). 154 See my mention of NMDA effects in chapter 7. There my example was correcting offcourse arm trajectories, but it equally applies to subvocal sequences. 155 A good physiologically oriented book on music is by the neurologist Frank R. Wilson, Tone Deaf and All Thumbs? (Viking Penguin 1986). The illustration showing the bifurcating path of a pendulum attracted by several magnets was made using James Gleick's CHAOS: The Software (Autodesk 1991). 157 John Holland, "Complex adaptive systems," Daedalus (Winter 1992), p. 25.

Chapter 10. The Making of Metaphor 159 Samuel P. Huntington, "If not civilizations, what?" Foreign Affairs 72(5):186-194 (1993). 159 Michael Reddy, "The conduit metaphor," in A. Ortony (ed.), Metaphor and Thought (Cambridge University Press 1979). 159 The art of the good guess is discussed by Calvin (1996). 159 Allan Sandage, quoted by Timothy Ferris in The New Yorker, p. 50 (15 May 1995). 160 "Without imagination...": Harold Osborne, Aesthetics and Art Theory (Dutton 1970), p.208. 161 Freeman (1995), p. 107. 161 Schema is used for knowledge structures in general, but I am using it in Johnson's (1987, p.2) sense of an image schema, a dynamic pattern that functions somewhat like an abstract version of an image, thereby connecting up a vast range of different experiences that manifest similar properties. 161 My grammar exposition derives from that of Derek Bickerton, Language and Species (University of Chicago Press 1990). In human language cortex, the layer 3 pyramidal neurons are consistently larger in the left hemisphere: J. J. Hutsler, M. S. Gazzaniga, "Acetylcholinesterase staining in human auditory and language cortices: regional variation of structural features," Cerebral Cortex 6:260-270 (April 1996). 161 Containment, see Johnson (1987), p.126. 162 P. Iverson, Patricia K. Kuhl, "Mapping the perceptual magnet effect for speech using signal detection theory and multidimensional scaling," Journal of the Acoustical Society of America 97:553-562 (1995). 163 Nancy J. C. Andreasen, Pauline S. Powers, "Creativity and psychosis: An examination of conceptual style," Archives of General Psychiatry 32:70-73 (1975). 164 Dedre Genter, Donald Genter, "Flowing water or teeming crowds: mental models of electricity," in Dedre Genter and Albert Stevens (eds.), Mental Models (Erlbaum 1983), pp.99-129. 164 Hans Selye, see Johnson (1987), chapter 5. 165 Marvin Minsky, The Society of Mind (Simon & Schuster 1987), ch. 20. 166 "One then reduces the excitability until only the better resonances remain active." This is not unlike reducing the temperature in the DNA annealing technique, judging the percentage of zipped-up DNA fragments from the temperature at which the solution's surface first coalesces. 166 Henry Moore, quoted at p.26 by Ken Macrorie, Telling Writing, 3d ed. (Hayden Book Company 1980). 167 Note that if a spatiotemporal pattern did not need to be spatially cloned, in order to gain the attention of output pathways, the spatial extent of attractors could be less than a hexagon pair. But that would give a lot of power to very few cells, and a chorus requirement would be safer. 169 I have discussed the common neural machinery for speech and hand movements most recently in William H. Calvin, "The unitary hypothesis: A common neural circuitry for novel manipulations, language, plan-ahead, and throwing?" pp. 230-250 in Tools, Language, and Cognition in Human Evolution, edited by Kathleen R. Gibson and Tim Ingold (Cambridge University Press 1993). 169 "Vice versa...." Calvin (1993). 170 George A. Ojemann, "Brain organization for language from the perspective of electrical stimulation mapping," Behavioral and Brain Sciences 6(2):189-230 (June 1983). 170 Bickerton (1990), p.86. 170 Jacob Bronowski, The Origins of Knowledge and Imagination (Yale University Press 1978, transcribed from 1967 lectures). 171 Kenneth J. W. Craik, The Nature of Explanation (Cambridge University Press 1943). 172 Narrative unity: see, for example, Paul Ricoeur, Time and Narrative (University of Chicago Press 1984). 172 Heinz Pagels, The Dreams of Reason (Simon & Schuster 1988).

Chapter 11. Thinking a Thought in the Mosaics of the Mind 175 Daniel C. Dennett, Darwin's Dangerous Idea (Simon & Schuster 1995), p. 460. And, since I did promise you the answer to Dennett's puzzler, X is: Pdun Dqwrqb'v idprxv ixqhudo rudwlrq lq Zlooldp Vkdnhvshduh'v Mxolxv Fdhvdu, Dfw LLL Vfhqh 2: "Iulhqgv, Urpdqv, frxqwubphq, ohqg ph brxu hduv; L frph wr exub Fdhvdu, qrw wr sudlvh klp." Well, to keep you from involuntarily seeing the answer, I've encrypted it with the famous Caesar Cipher where each plaintext character is replaced by the one located three to the right in modulo 26. I've left the number and the punctuation unencrypted. ABCDEFGHIJKLMNOPQRSTUVWXYZ plaintext DEFGHIJKLMNOPQRSTUVWXYZABC ciphertext 176 Karl R. Popper and John C. Eccles, The Self and Its Brain (Springer 1977) 176 Eugen Herrigel, Zen in the Art of Archery (Pantheon 1953). 180 Jonathan Weiner, The Beak of the Finch (Knopf 1994), p. 129. 181 J. B. S. Haldane, Journal of Genetics 58 (1963). 181 For a history of the confusions about levels of explanation and mechanism, see Helena Cronin, The Ant and the Peacock (1991). 181 Ignorance of levels of explanation: see my How Brains Think, chapter three, "The janitor's dream." 181 William James, Principles of Psychology (1890). 182 Francis Crick and Christof Koch, ``The problem of consciousness,'' Scientific American 267(3):152-159 (September 1992). The Neural Correlate of Consciousness (their NCC) is some relevant group of neurons firing in some relevant pattern for a sufficient duration. It is easy to imagine how population-style hegemony could be their NCC, but I would caution that passive awareness may be much simpler than the creative constructs implied by the James-Piaget-Popper levels of consciousness; a pop-through recognition of a familiar object may not need to utilize a cloning competition in the manner of an ambiguous percept or a novel movement. 183 Edelman (1989), p. 148. 183 Paul Valéry, quoted at p. 346 in W. H. Auden and L. Kronenberger, The Viking Book of Aphorisms (Viking 1962). 183 Dreaming: Hobson (1988). 185 "Too slow." One of our best ways of compensating for insufficient amounts of neurotransmitters is to increase the time it dwells in the synaptic cleft. But drugs that delay transmitter breakdown or sequestration thereby change the time constants, and so slow the natural fluctuations. 186 Kay Redfield Jamison, An Unquiet Mind: A Memoir of Moods and Madness (Knopf 1995). 186 Mixed depression: Frederick K. Goodwin, Kay Redfield Jamison, Manic-depressive Illness (Oxford University Press 1990), p.48. 187 Hobson (1994). 187 Hebb (1980), p. 26. 188 Joan of Arc: Calvin & Ojemann (1994), p. 79. 188 "Some long-ago success" might, at one extreme, be the tuning-up period of ontogeny when diffuse wiring is pruned, leaving only those terminal clusters that have been engaging in a test pattern. 189 Functional roles for EEG rhythms: discussed by Theodore H. Bullock,"How do brains work?" chapter 10 in Induced rhythms in the brain, edited by E. Basar, T. H. Bullock (Birkhauser 1991). 189 Wallace Stevens, from "Adagia," in Opus Posthumous (Knopf 1957). 191 Our modern experience with packet data transmission illustrates one way that a serial-order bottleneck can be circumvented, allowing the same channel to be simultaneously used for several tasks (internet telephony, text file transfer, and image download, all going over the same twisted pair wire). Frequency multiplexing is another, as is time slicing. So until we have pushed the issue hard enough with experimental techniques, it may be well to remember that the "unity of consciousness" is not the settled issue that it first appears. 191 Attractors that fade more slowly might still fade out overnight, provided that sleep processes protected the cortical area from writing new ones. REM sleep process do, after all, inhibit many muscles; also inhibiting the cortical areas used for agendas might function much like the mantras of my Intermission Notes. 192 George Steiner, "Has truth a future?" Bronowski memorial lecture, reprinted in Bernard Dixon, editor, From Creation to Chaos (Basil Blackwell 1989), pp. 234-252 at p.250. Simply "being interested in something," as Steiner likes to say, is a form of evolving agenda that structures the daily lives of creative people. There are likely multiple evolving agendas in no particular hierarchy, as when one interrupts writing the magnum opus to do the laundry -- and then again, an hour later, when one remembers to water the dehydrated house plants. 194 Bickerton (1990). For some of the elements needed for a Universal Grammar, see Jackendoff (1993), p. 81, pp. 159-164; Bickerton (1995), pp.30ff; and Noam Chomsky, "A minimalist program for linguistic theory," pp. 1-52 in The View from Building 20 (MIT Press 1993), edited by K. Hale and S. J. Keyser (it's a WW2 "temporary building" at M.I.T.; back in 1961-62, I had an office in 20B-225). It is thought that a mechanism for recursive embedding buys you the most important aspects of UG. 196 William H. Calvin, "The emergence of Universal Grammar from protolanguage: corticocortical coherence could enable binding and recursive embedding," Society for Neuroscience Abstracts 22 (1996). 199 Darwin (1859).

Glossary and Brief Tutorials 203 See Stewart (1995), p.117. 204 For more on chaos, start with chapter 8 of Stewart (1995) before progressing to Abraham (1990), Glass and Mackey (1990), and Freeman (1995). 206 Discussions of unitary processes can be found in William H. Calvin and Katherine Graubard, "Styles of neuronal computation," chapter 29 in The Neurosciences, Fourth Study Program, edited by F. O. Schmitt and F. G. Worden (MIT Press 1979). 206 Helena Cronin, The Ant and the Peacock (Cambridge University Press 1991), p.107. 206 Genetic code: see any biology text or Douglas Hofstadter Metamagical Themas (BasicBooks 1985), pp.672ff. 212 Resonance: see, for example, Stewart (1995), pp. 24-25.