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Aug 17, 2012 - John Gardiner. To cite this article: John Gardiner (2012) Insights into plant consciousness from neuroscience, physics and mathematics: A role ...
Plant Signaling & Behavior

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Insights into plant consciousness from neuroscience, physics and mathematics: A role for quasicrystals? John Gardiner To cite this article: John Gardiner (2012) Insights into plant consciousness from neuroscience, physics and mathematics: A role for quasicrystals?, Plant Signaling & Behavior, 7:9, 1049-1055, DOI: 10.4161/psb.21325 To link to this article: http://dx.doi.org/10.4161/psb.21325

Published online: 17 Aug 2012.

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PerSPectiveS Plant Signaling & Behavior 7:9, 1049-1055; September 2012; © 2012 Landes Bioscience

John Gardiner The School of Biological Sciences; The University of Sydney; Sydney, Australia

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here is considerable debate over whether plants are conscious and this, indeed, is an important question. Here I look at developments in neuroscience, physics and mathematics that may impact on this question. Two major concomitants of consciousness in animals are microtubule function and electrical gamma wave synchrony. Both these factors may also play a role in plant consciousness. I show that plants possess aperiodic quasicrystal structures composed of ribosomes that may enable quantum computing, which has been suggested to lie at the core of animal consciousness. Finally I look at whether a microtubule fractal suggests that electric current plays a part in conventional neurocomputing processes in plants.

Keywords: quasicrystal, gamma wave, consciousness, Orch-OR, microtubule Abbreviations: ADNP, activity-dependent neuroprotective protein; CDK5, cyclin-dependent kinase 5; CRMP, collapsing response mediator protein; LTP, long term potentiation; MAP, microtubule-associated protein; NAP, NAPVSIPQ; NMDA, N-methyl-Daspartic acid; Orch-OR, orchestrated objective reduction; PKA, protein kinase A; TTBK1, tau-tubulin kinase 1 Submitted: 05/11/12 Revised: 07/01/12 Accepted: 07/02/12 http://dx.doi.org/10.4161/psb/ *Correspondence to: John Gardiner; Email: [email protected]

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Introduction The question of whether plants are conscious is not a trivial one. On it depends much concerning our relationship with the natural world. Some religious traditions such as Jainism suggest plants are conscious while others, including Buddhism, deny they are conscious. A number of definitions of consciousness exist, including “Not just animals are conscious but every organized being is conscious. In the simplest sense, consciousness is an awareness (has knowledge) of the outside world”1 cited in reference 2. The latest thinking on plant consciousness suggests that “root brains” may participate in the creation of a swarm-like intelligence.3 Nonetheless there must be mechanisms by which the input from each “root brain” is integrated into a holistic response by the plant. Here

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I look at recent developments concerning consciousness in animals, including the importance of the microtubule cytoskeleton and gamma waves, and investigate whether they may be relevant to possible consciousness in plants. In particular I focus on the work of Roger Penrose, the mathematician, who has suggested that our lack of understanding of animal consciousness is due to our lack of understanding of quantum mechanics. I then look at how quantum mechanics may interact with plant form and function. Consciousness and memory According to Crick “some form of very short-term memory seems almost essential for consciousness, but this memory may be very transient, lasting for only a fraction of a second.”4 To be conscious of something at the time it occurs, that information must be represented in working memory at the same time. It appears that we have conscious access to information processing when it occurs in areas with connections to the working memory circuitry of the prefrontal cortex.5 Thus there is a strong connection between working memory and consciousness, and it appears that gamma synchrony and microtubules may play a key role in both.6,7 Drug studies suggest a role for microtubules in memory formation in animals. Rats with dorsal dentate gyrus dysfunction induced by the microtubule-depolymerising agent colchicine lesions show severe impairment in disambiguating objects, an important aspect of event memory.8 In the Morris water-maze learning test, colchicine induced memory impairment

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Insights into plant consciousness from neuroscience, physics and mathematics: A role for quasicrystals?

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neuronal synaptic plasticity, and synaptic plasticity plays a crucial role in learning, memory, and cognitive disorders. Stable isotope labeling can measure the turnover of tubulin in defined microtubule populations in the murine brain. Basal turnover was highest in Tau-associated microtubules, intermediate in MAP2-associated microtubules and lowest in cold-stable microtubules. Contextual fear conditioning, a hippocampus-mediated form of memory formation, was accompanied by an increase in the turnover of tubulin in MAP2 and cold-stable microtubules. Treatment with the microtubule-depolymerising drug nocodazole impaired memory formation and this could be reversed by the microtubule-stabilizing drug taxol or BDNF.18 Social isolation from weaning affects hippocampal structure and function in the rat. Thus, isolated rats showed recognition memory deficits in the novel object recognition task. These behavioral alterations were accompanied by alterations in hippocampal α-tubulin isoform expression consistent with microtubule stabilization.19 Expression of different tubulin isotypes during development is likely to modulate microtubule function.20 Memory in plants. Do microtubules in plants play a role in memory formation as in animals with a nervous system? Microtubules in cold-tolerant wheat become acclimated to cold-shock following chilling or after treatment with abscisic acid.21 One way this may occur is through differential tubulin isotypes.22 This suggests that indeed plant microtubules can also encode memories, as in animals. However, perhaps not all plant cells can perform this role. Microtubules in Arabidopsis epidermal hypocotyls undergo slow rotary movements in clockwise or counter-clockwise rotation.23 This means that long-term memory storage in these microtubule arrays is unlikely due to the continuously shifting nature of their interaction with other cellular compartments, including plasmodesmata. Microtubules in plants are also more dynamic than those of animals.24 Plants possess other forms of memory as well. For example, plants display transcriptional stress memory25 and epigenetic processes are important during vernalisation.26 It remains to be seen whether memory in

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plants plays a role in consciousness as it is suggested to in animals. Gamma and Theta Waves, Memory and Microtubules A gamma wave is a pattern of neural oscillation in humans with a frequency between 25 to 100 Hz, though 40 Hz is prototypical.27 The microtubule cytoskeleton may play a role in gamma-synchorny as the MAP connexin 43 links the microtubule cytoskeleton28 to gap junctions, which are crucial in the generation of gamma synchrony. Both gamma-synchrony and microtubule function are important for the development of consciousness. Anesthetics are known to disrupt microtubules and induce memory loss, although they also affect other cellular components including loss of membrane constituents.29 Anaesthesia may act on microtubules in a number of ways. They may act by van der Waal’s forces on hydrophobic pockets in proteins, including hydrophobic pockets in tubulin proteins. Quantum effects mediated by endogenous van der Waal’s forces in hydrophobic pockets of select proteins may be required for consciousness.30 Notably, however, anesthesia affects Tau protein, inducing phosphorylation of Tau protein31 and causing the detachment of 3-repeat Tau protein from microtubules in transgenic mice without affecting microtubule structure.32 During mental practice, long-term meditators induce high-amplitude gamma synchrony, suggesting that higher-level mental states are dependent upon gamma synchrony.33 Gamma synchrony is important in the formation of memories. If synaptic connections between synchronously firing neurons can be modified by spike-timing-dependent plasticity, then an increase in synchronicity between these neurons may induce long-term potentiation of these synapses. As a result, the stimulus properties that have activated these neurons are associated with each other to form a new memory.34 There are interactions between microtubules and gamma synchrony. Tau protein, a neuronal MAP implicated in microtubule stabilization and axonal elongation during neuronal development, is expressed at high levels in neocortical

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even at a dose at which there was no evidence of any histological changes in the dentate gyrus cells, suggesting that the effect is non-toxic.9 Continuous microtubule disruption by colchicine resulted in a dose-dependent learning deficit in rats.10 Similarly, bilateral infusion of colchicine into the fimbria of the rat brain caused a transient impairment in radial-arm maze performance whereas unilateral infusion did not.11 MAPs (microtubule-associated proteins) are important during learning in animals. In mice expressing Tau-tubulin kinase 1, which phosphorylates Tau protein, there is a significant age-dependent memory impairment. TTBK1 in the Azheimer’s disease brain may be one of the underlying mechanisms inducing activation of CDK5 and calpain, downregulation of NMDA receptor type 2B, and subsequent memory dysfunction.12 Blocking the Ser(238) and Thr(245) phosphorylation sites on Tau protein in Drosophila causes strongly impaired associative learning.13 NAP (NAPVSIPQ) is a peptide derived from activity-dependent neuroprotective protein (ADNP) that interacts with microtubule and provides neuroprotection. NAP treatment partially ameliorates cognitive deficit and Tau hyperphosphorylation in ADNP(+/-) mice.14 MAP2 targets PKA to microtubules. PKA binding to MAP2 and MAP2 phosphorylation is essential for the selective development of contextual memory, since mice lacking the PKA binding site of MAP2 are impaired in conditioned freezing.15 Rats trained in a novel context show significantly increased immunostaining for MAP2. This increase was observed two weeks after training and was selective for hippocampal CA1 and CA2 pyramidal cells.16 CRMP (Collapsin Response Mediator Protein) -1(-/-) mice exhibit reduced and disorganized MAP2 staining in distal dendrites of hippocampal CA1 pyramidal cells. These mice show a reduction in LTP in the CA1 region and impaired performance in hippocampaldependent spatial learning and memory tests.17 Alterations in tubulin expression and turnover accompany learning in animals. Cytoskeletal reorganization underlies

Conciousness and Quantum Mechanics Relevance to quantum computing in the brain. Microtubule function and gamma synchrony have now been linked.35 This supports the Penrose-Hameroff “Orch-OR” model of consciousness whereby quantum computing in microtubules within dendrites and other regions linked by gap junctions occurs as gamma EEG-synchronised sequences of discrete quantum computational events.41 This model is, however, highly controversial and a number of authors have critiqued it.42 Here microtubules may form

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a Bose-Einstein condensate, allowing a large number of particles to be locked in phase and form a single quantum object, linked through gap junctions. It appears likely that MAPs, including Tau, may play a key role in this process, orchestrating the quantum processing of the microtubules again as suggested by Penrose-Hameroff. Other interactions of plants with quantum mechanics. Quasicrystals are structures that are ordered but not periodic. While traditional crystals can possess only two, three, four, and 6-fold rotational symmetries, quasicrystals possess other symmetry orders, for instance 5-fold. Aperiodic tilings were first discovered by mathematicians (Fig. 1), and aperiodic quasicrystals have since been found in nature including an alloy of aluminum, copper, and iron icosahedral quasicrystal with 5-fold symmetry.43 This naturallyoccurring quasicrystal has been subsequently suggested to have extraterrestrial origins, forming in the early solar system about 4.5 Gya.44 Roger Penrose, in his book The Emperor’s New Mind,45 suggests that quasicrystals require quantum mechanics in order to form. “Normally, when Nature seeks out a crystalline configuration she is searching for a configuration of lower energy… I am envisaging a similar thing with quasicrystal growth, the difference being that its state of lowest energy is much more difficult to find, and the ‘best’ arrangement of the atoms cannot be discovered simply by adding on atoms one at a time in the hope that each individual atom can get away with solving its own minimizing problem. Instead, we have a global problem to solve. It must be a co-operative effort among a large number of atoms all at once. Such co-operation, I am maintaining, must be achieved quantum-mechanically…” Astonishingly, Duckett in a 1972 paper46 discovered what appear to be quasicrystals in fertilised eggs from the fern Pteridium aquilinum. This consists of regular pentagonal arrays of ribosomes associated with the endoplasmic reticulum (Fig. 2). Ribosomes are molecular structures responsible for the catalysis of proteins from amino acids using mRNA as a template.47 Ribosomes are known to form clusters as rosettes, spirals, or circles48,49

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but can appear in other rare conformations as well. Here they clearly form a quasicrystal, with a local 5-fold symmetry but overall a crystal structure. Two different quasicrystal arrangements are visible here, with an angular arrangement on the left and a regular lattice on the right. Other endoplasmic reticulum membrane components may play roles as other “tiles” in the quasicrystal. To my knowledge, this is the first recorded instance of a quasicrystal found in a living organism. It will be of great interest to investigate whether other organisms may also possess ribosomal quasicrystals and to investigate the molecular mechanisms behind the formation of these quasicrystals in Pteridium aquilinum eggs. As discussed above, quantum mechanical mechanisms may play a role here. This is exciting as it extends the number of recorded instances where quantum mechanics is involved in plant growth and development and indeed quantum coherence has been shown to play a role elsewhere in plants during photosynthesis.50 Microtubules can Function as Biological Wires Both microtubules act as biological electric wires that can transmit and amplify electric signals via flow of condensed ion clouds. Taxol-stabilized MTs behave as biomolecular transistors, capable of amplifying electrical information.51 Both the tubulin C-terminal tail regions and the nano-pore openings lining the microtubule wall are important here. Thus, ions may flow along and through microtubules in the presence of potential differences, thus propagating intracellular signaling.52 It is suggested that MAPs, including MAP2, may cause perturbations in the local electrostatic field that propagate over distances greater than those between adjacent microtubules. This may enable MAPs to potentially act as a biological wires transmitting current from one microtubule to another.53 This is likely to play a key role in animal conventional neurocomputing, as opposed to quantum computing and indeed recent work suggests that microtubules can store huge amounts of memory encoded in phosphorylated tubulin subunits.54

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regions and the hippocampus. Due to this localization Tau might play a role in neural responses underlying slow and fast brain oscillations and long-range synchronisation between the hippocampus and neocortex. Indeed Tau -/- mice show hippocampal theta slowing and reduced level of gamma long-range synchronisation involving the frontal cortex.35 This study for the first time links the two major concomitants of consciousness and memory formation: gamma wave oscillations and microtubule function. Interestingly, electrical stimulation of rat brains at 50Hz (within the range of gamma waves) caused an upregulation of MAP2 while this did not occur with 250Hz stimulation.36 This suggests a possible feedback situation between microtubule stabilization and gamma synchrony. Do plants possess gamma waves? It is not known whether plants possess electrical signaling processes that result in gamma wave-like activity. They have been shown to exhibit neuroid conduction (the propagation of electrical events in the membranes of non-nerve and non-muscle cells) similar to that seen in simple animals with synchronous electric activities of root cells emerging in a specific root apex region37 and action potentials propagate from root to shoot or shoot to root.38 Indeed plant plasmodesmata may be homologous structures to animal gap junctions,39 which are essential for the propagation of gamma waves. Plasmodesmata are also known to interact closely with the microtubule cytoskeleton,40 as do gap junctions during gamma synchrony.

Microtubules and electric current in plants. It is likely that plant microtubules also conduct electrical current. Interestingly, microtubules recovering from depolymerisation in Nitella form branched, fractal-like structures (Fig. 3a).55 These appear similar to Lichtenberg figures, which are fractal branching electrical discharges (Fig. 3b). Indeed electric current seems to favor the formation of branched fractals with non-equilibrium electrodeposition of metals also creating branched fractals (Fig. 3c).56 Thus electrical current flowing through microtubules

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may play a role in the branched microtubule arrays of Nitella and possibly in other plants as well. Conclusions I have examined the role of gamma waves, microtubules and quantum mechanics in the possible development of consciousness in plants. Much more work needs to be done here. A good starting point would be to investigate whether plants possess gamma waves using EEG. Even if they do not, however, other forms of electrical

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linkage between cells may fulfil the role of gamma waves in promoting consciousness. Further understanding of consciousness in animals in the future will hopefully translate into greater understanding of plant consciousness as well. References 1. Margulis L, Sagan D. What is life? New York, NY, USA, Simon and Schuster, 1995. 2. Trewavas AJ, Baluška F. The ubiquity of consciousness. EMBO Rep 2011; 12:1221-5; PMID:22094270; http://dx.doi.org/10.1038/embor.2011.218. 3. Baluška F, Lev-Yadun S, Mancuso S. Swarm intelligence in plant roots. Trends Ecol Evol 2010; 25:6823; PMID:20952090; http://dx.doi.org/10.1016/j. tree.2010.09.003.

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Figure 1. An example of a pentagonal aperiodic Penrose tiling.

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Figure 2. tangential section through the membranes of a stack of endoplasmic reticulum showing regular pentagonal quasicrystal of ribosomes. From.46 18. Fanara P, Husted KH, Selle K, Wong PY, Banerjee J, Brandt R, et al. Changes in microtubule turnover accompany synaptic plasticity and memory formation in response to contextual fear conditioning in mice. Neuroscience 2010; 168:167-78; PMID:20332016; http://dx.doi.org/10.1016/j.neuroscience.2010.03.031. 19. Bianchi M, Fone KF, Azmi N, Heidbreder CA, Hagan JJ, Marsden CA. Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. Eur J Neurosci 2006; 24:2894-902; PMID:17116162; http://dx.doi. org/10.1111/j.1460-9568.2006.05170.x. 20. Tischfield MA, Engle EC. Distinct alpha- and betatubulin isotypes are required for the positioning, differentiation and survival of neurons: new support for the ‘multi-tubulin’ hypothesis. Biosci Rep 2010; 30:319-30; PMID:20406197; http://dx.doi. org/10.1042/BSR20100025. 21. Wang QY, Nick P. Cold acclimation can induce microtubular cold stability in a manner distinct from abscisic acid. Plant Cell Physiol 2001; 42:999-1005; PMID:11577195; http://dx.doi.org/10.1093/pcp/ pce135. 22. Kerr GP, Carter JV. Tubulin isotypes in rye roots are altered during cold acclimation. Plant Physiol 1990; 93:83-8; PMID:16667471; http://dx.doi. org/10.1104/pp.93.1.83. 23. Chan J, Calder G, Fox S, Lloyd C. Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat Cell Biol 2007; 9:1715; PMID:17220881; http://dx.doi.org/10.1038/ ncb1533.

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Figure 3. (A) Microtubule arrays in Nitella form branched arrays on recovery from depolymerisation. 55 (B) this 3” x 3” x 2” three dimensional Lichtenberg Figure was created by ebeam irradiation along multiple planes. the internal potential within the specimen prior to discharging it was estimated to be 2.2 million volts. the specimen is illuminated from below by blue LeDs. (c) electrodeposition of metals causes dedritic structures to form.56

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