Download Article - Saha Institute of Nuclear Physics

Learning & Intelligence of Plants:
Developments following Jagadish Chandra Bose Rahul Banerjee and Bikas K. Chakrabarti
Rahul Banerjee is a Professor in the Crystallography and Molecular Biology Division of the Saha Institute of Nuclear Physics, Kolkata. His research interests include protein crystallography and plant intelligence.
Bikas K. Chakrabarti is a Senior Professor (Physics) of the Saha Institute of Nuclear Physics and Visiting Professor (Economics) of Indian Statistical Institute, Kolkata. His research interest includes studies on complex neural and other networks.
1. Introduction
In the history of Indian science the realm of plant signaling and Jagdish Chandra Bose occupies an information processing. Although in unique position. Seldom do we find a his time many of his ideas received a scientist equally at home in wide hostile reception from certain range of disciplines ranging from quarters, it is now a fact that most of physics, instrumentation and botany. them have been absorbed into the This article reviews the seminal mainstream, current scientific contributions of Bose in the realm of literature.
to the stem, and its passage through the stem (in both up and down directions) caused the other leaves to collapse. Similar experiments confirmed the coupling of electrical oscillations and spontaneous leaf movements in Desmodium. These movements could be discontinued by a cut in the Desmodium stalk, which plant biophysics and also the current Contributions of Bose
could again be restored by the developments in line with his ideas. In Bose's view (see box 1) there was passage of an electric current through Finally, the paper concludes with a physical/computational model of an essential unity in the physiological the pulvinus. In addition, the plant learning inspired by Jagdish mechanisms in both animal and crescograph was used to demonstrate Chandra. The past decade has seen a plants such that, “There is no the pulsatory nature of the growth in significant number of plant scientists physiological response given by the D e s m o d i u m a n d i t s d i r e c t affirming the basic insights of Bose in most organized animal tissues that is correspondence with electrical also not met with in a simpler form in activity. Description of the most plants” [1]. Further, plants were elegant experiments related to the endowed with a certain degree of ascent of sap lies outside the scope of individuality and any experiment this article, yet even here Bose was involving plants would have to take able to show the correlation between note of their past history and the variability in turgor pressure consequent present response [2] . By with electrical signals [4]. These and means of the Resonant Recorder and a host of other experiments led Bose the Electric Probe (both instruments to conclude that plants, like animals designed by him along with the are in possession of a nervous system Crescograph [3] ), Bose was able to (though primitive), and similar to demonstrate that the collapse in the animals, the response of the whole leaves of the Mimosa plant (Fig. 1) plant to stimuli was a consequence of A Bronze Plaque of Acharya J.C. Bose – working upon stimulation was accompanied long range electrical signaling with Magnetic Chrescograph. (Courtesy : Bose Institute, Kolkatta)
by an electrical signal which traveled through out the entire plant body.
57
Instrumental Design and Views of J. C. Bose J. C. Bose was unique in that he not only designed and fabricated his own instruments to study plant response to stimuli but also gave a series of biological insights spanning the plant and animal kingdoms. Given in this box are two excerpts from the writings of Acharya J. C. Bose; one concerned with the design of the crescograph and the other dealing with his philosophical views on inanimate and living matter, to demonstrate his equal ability in instrumental design and original theory. “ The magnification in my Crescograph is obtained by a compound system of two levers. The growing plant is attached to the short arm of a lever, the long arm of which is attached to the short arm of the second lever. If the magnification by the first lever be m, and that by the second, n, the resulting magnification is mn.
The practical difficulties met with in carrying out this idea are very numerous. It will be understood that just as the imperceptible movement is highly magnified by the compound system of levers, the various errors and difficulties are likely to be magnified in the same proportion. The principal difficulties met with were due to : 1) to the weight of the compound lever which exerted a great tension on the growing plant, 2) to the yielding of flexible connections by which the plant was attached to the first lever, and the first lever to the second, and 3) to the friction at the fulcrums.
Weight of the lever: - As the first lever is to exert a pull on the second , it has to be made rigid. The second lever serves as an index, and can therefore be made of fine glass fibre. The securing of rigidity of the first lever entails large cross section and consequent weight, which exerts considerable tension on the plant. Excessive tension greatly modifies growth; even the weight of the index used in self – recording auxanometers is found to modify the rate of growth. The weight of the levers introduces an additional difficulty in the increased friction at the fulcrums, on account of which there is an obstruction of the free movement of the recording arm of the lever. The conditions essential for overcoming these difficulties are 1) construction of a very light lever possessing sufficient rigidity, and 2) arranging the levers in such a way that the tension on the plant may be reduced to any extent, or even eliminated.
I found in navaldum, an alloy of aluminium a light material possessing sufficient rigidity. The first lever is constructed out of a thin narrow sheet 25 cm. in length; it has, as explained before, to be fairly rigid in order to exert a pull on the second without undergoing any bending; this rigidity is secured by giving the thin narrow plate of the lever a T – shape. The first lever balances, to a certain extent , the second. Finer adjustments are made by means of an adjustable counterpoise B, at the end of the levers. By this means the tension on the plant can be greatly reduced; or a constant tension maybe exerted by means of a weight T. In my later type of the apparatus the plant connection is made to the right, instead of the left side of the first fulcrum. This gives certain practical advantages. The second lever is then made practically to balance the first, only a slight weight being necessary for the exact counterpoise. The reduction of total weight thus secured reduces materially the friction at the fulcrum with great enhancement of the efficiency of the apparatus.'
[ From The high magnification crescograph for researches on growth, Bose, J. C. From : Acharya J. C. Bose – A scientist and a dreamer Vol. 1 (1996) Eds. P. Bhattacharyya & M. Engineer, Bose Institute , Calcutta, pp. 465 – 467, (1996)]
“ In the pursuit of my investigations I was unconsciously led into the border region of physics and physiology and was amazed to find boundary lines vanishing and points of contact emerge between the realms of the living and the Non – living. Inorganic matter was found anything but inert; it was also a – thrill under the action of multitudinous forces that played on it. A universal reaction seemed to bring together metal, plant and animal under a common law. They all exhibited essentially the same phenomenon of fatigue and depression, together with possibilities of recovery and exaltation, yet also that of permanent irresponsiveness which is associated with death. I was filled with awe at this stupendous generalization; and it was with great hope that I announced my results before the Royal Society, - results demonstrated by experiments. But the physiologists present advised me, after my address, to confine myself to physical investigations in which my success had been assured , rather than encroach on their preserve. I had thus unwittingly strayed into the domain of a new and unfamiliar caste system and so offended its etiquette. An unconscious theological bias was also present which confounds ignorance with faith. It is forgotten that He, who surrounds us with this ever – evolving mystery of creation, the ineffable wonder that lies hidden in the microcosm of the dust particle, enclosing within the intricacies of its atomic form all the mystery of the cosmos, has also implanted in us the desire to question and understand. To the theological bias was added the misgivings about the inherent bent of the Indian mind towards mysticism and unchecked imagination. But in India this burning imagination which can extract new order out of a mass of apparently contradictory facts, is also held in check by the habit of meditation. It is this restraint which confers the power to hold the mind in pursuit of truth, in infinite patience, to wait, and reconsider, to experimentally test and repeatedly verify.”
[The voice of life, Bose, J. C. From : Acharya J. C. Bose – A scientist and a dreamer Vol. 4 (1996) Ed. P. Bhattacharyya, Bose Institute , Calcutta, pp. 60 – 62, (1996)]
58
Figure 1(a): Mimosa Plant with leaves open. along the ground in search of darkness probably caused by the shadow of a prospective host tree, called skototropism. Every tropism however, involves three distinct phases, 1) the detection of the initial environmental signal by plant receptors 2) subsequent processing/transduction of the primary signal and 3) the consequent integrated physiological response. Plants being sessile (that is literally rooted to the same spot), the response is more in terms of growth and development in contrast to animals who respond primarily by movement. Whatever the tropism, the resulting responsive growth invariably involves the asymmetric redistribution of the plant hormone auxin. Even though all tropisms will most probably involve auxin yet the receptor and the suite of molecules involved in the transduction of the signal are quite different in each case. Currently a plethora of plant hormones have been discovered apart from auxin (gibberelic acid, cytokinin, sugars, brassinosteroids), with interlinked signaling pathways.
A detailed description of the receptors and their associated signaling pathways for the different tropisms lies beyond the scope of this article. Rather we will only discuss thigmotropism (response due to touch) as it relates to the extensive work of Bose on the Mimosa plant. The primary receptor for touch (if it at all exists) is yet to be identified. However, there is no doubt that the second most important messenger is intracellular calcium (Ca2+). The electrical signal 1(b) The leaves fold and droop when touched
which is an action potential, thus generated (measured by Bose in Mimosa) is 2+
Figure 1 A Mimosa plant before and after touch due to the rapid increase in cellular calcium (Ca ) in the mechanically stimulation. Bose made a detailed study of the perturbed cells [5]. Unlike animal cells which utilize Na+ and K+ ions, action electrical signaling involved in the collapse of potentials in plants require the dynamical redistribution of Ca2+, K+ and Cl- the leaves in the Mimosa plant ( Bose, J. C. The nervous mechanism of plants. (1926)Longmans ions. The action potential generated in the Mimosa leaflet travels to the Green & Co., London. pp. 40.). Other pulvinus with a speed of about [6] 20 – 30 mm/s. Bose had measured [2] the experiments led him to conclude that electrical speed of transmission to be about 30 mm/s . In comparison the action potential signals were also coupled to the movements of transmission speeds in the case of Anodonta is 45 mm/s, slug (125 mm/s), the leaf in Desmodium (Bose, J. C. Researches on the irritability of plants. (1913) Longmans, octopus (3000 mm/s) and in mammals up to 100,000 mm/s. On reaching a Green & Co., London. pp. 94 ). pulvinus the action potential is transmitted laterally via plasmodesmata into P h o t o s b y B a r r y R i c e , P h D ; the cells of the motor cortex which respond by ion and water efflux leading to http://www.sarracenia.com/galleria/galleria.ht
the dramatic leaf movements in Mimosa.[6] The initiation of the action ml potential and the subsequent signal transduction steps leading to ion and water Plant Tropisms efflux in the motor cortex requires further elucidation in terms of molecular The directed response of a plant due to environmental stimuli is termed as tropism, to be distinguished from nastic movements which occur spontaneously without a definite relation to any environmental stimulus vector. Thus, response to the direction of light is termed phototropism, due to gravity gravitotropism, touch – (a)
(c)
(b)
thigmotropism and water - hydro tropism . There is also the most Figure 2 : A Venus Fly Trap before and after entrapping an insect. Two successive electrical signals precede the closing of the trap around the insect (Simons, P. J. The role electricity in plant movements. (1981) New unusual tropism of the parasitic Phytologist, 87, pp. 11 – 37).Photos by Barry Rice, PhD; http://www.sarracenia.com/galleria/galleria.html
creeper vine Monstera which grows 59
events. Yet a set of touch inducible Plant neurobiology
genes (TCH) have been identified It thus appears we have turned a full Arabidopsis Thaliana, a significant circle. Initially, electrical signaling fraction of which encodes calcium was set aside in favor of the concept binding calmodulin or calmodulin - of 'chemical diffusion' of auxin which like proteins. This was probably only was thought to predominantly to be expected as the cellular m
ediate plant physiological distribution of Ca2+ plays a key role response. It now transpires that in the genesis and passage of action calcium signaling involving electrical potentials in the first place. The most signals could play the primary role dramatic thigmotropic response is in [7], with auxin transport based on a the case of the Venus fly trap (Dionaea vesicle – based process, rather like muscipula), a predatory plant which neurotransmitter release at synaptic closes its bilobed leaves around junctions in animal nervous systems. unsuspecting insects (Fig. 2), who So strong has been the returning wave mechanically disturb the trigger hairs that there has been definite proposals on its leaf surface. It is an interesting for a 'plant neurobiology [8] , a fact that two successive action discipline whose field of study potentials are required for leaf would seek to understand how plants closure. receive multiple environmental A c t i o n p o t e n t i a l s & signals, how these are processed by signal transduction networks and variational potentials
how these multiple yet interrelated There are actually two forms of information processing streams are electrical signals prevalent in plants integrated to yield the final the action potentials (AP) and the coordinated response . Brenner et al. slow wave variational potentials [8] sums up the objectives of the (VP). In contrast to the action nascent science as, “Plant potentials, the VP's vary with the neurobiology is a newly initiated field intensity of the stimulus (thereby of research aimed at understanding having a large range of variation how plants perceive their unlike AP's which are all or none) and circumstances and respond to have delayed repolarizations. The environmental input in an integrated ionic mechanism behind the fashion, taking into account the transmission of AP's also differ combined molecular, chemical and significantly from VP's. Both AP's electrical components of intercellular and VP's are involved in long – plant signaling. Plant neurobiology distance signaling and can invoke a is distinct from the various disciplines response distant from the local area of within plant biology in that the goal of the applied stimulus [6]. Thus AP's plant neurobiology is to illuminate have been implicated in trap/tentacle the information network that exists in closure (for Dionaea, Drosera), plants.”
regulation of leaf movements (Mimosa) , increase in respiration and This approach however, has not been gas exchange (Zea), decrease in stem without detractors. In a strongly growth (Luffa) and induction of gene worded article Alpi et al. [9] rejects expression (Lycopersicon). Similar the scope and validity of the new and other unique functions have been discipline on the grounds that plants do not have neurons or brains, in
identified for VPs [6].
short a nervous system. Again neurotransmitters are not transported from cell to cell as in the case of auxin, whose vesicular transport remains to be conclusively established. Another problem appears to be the existence of numerous plasmodesmata, apparently contributing to polar auxin transport between cells. In response, [ 8,10] the protagonists for 'plant neurobiology' contend that the term is used only as a metaphor, which under the present circumstances is highly apt. It is factually incorrect to suppose that existence of brains or nerves (literally speaking) is being proposed in plants. It is beyond any doubt that long–range electrical signaling does exist in plants and the mechanism by which a sunflower plant conducts an action potential over 0.3 m [8] remains to be elucidated in sufficient detail. As mentioned previously, much work remains to be done in understanding the role of electrical signals and their integration with plant chemical signaling systems. In such a situation where else to seek for analogies if not in animal neural models ? In this context it is notable that Bose [2] was the first to use the term 'plant nerve' and currently the plant phloem [8] has been compared to an animal axon in that both are capable of conducting bioelectrochemical impulses over long distances and being structurally equivalent to “hollow tubes filled with electrolyte solutions.”
The information processing network(s) in plants
The question then arises as to what constitutes the information processing network in plants analogous to the neural networks of animals ? 60
Any network will be composed of interplay of both leading to the other factors which are yet to be elements which are in specific regulation of plant physiology. In determined. By now it should be communication with each other. In network terminology, Ca2+ is a highly evident that the information network animal neural nets, the elements are connected hub as it is i) the corner in plants is quite complex and of course neurons interacting with stone of intra–cellular signal modeling this network to account for each other via synaptic junctions. transduction pathways ii) implicated plant physiological response could What could be the analogous in long distance electrical signals and well be a daunting task.
pathways of information flow in also iii) interacts with the chemical Calcium signaling and the plants? Plants lack specialized signaling systems. neuronal cells, yet information flows At the next level are directed Ca2+, K+, concept of 'calcium signature'
by electrical and chemical means Cl- ion fluxes which give rise to AP's or As calcium ion Ca2+ is implicated in through different levels of its VP's traveling over large cellular all forms of electrical and chemical structural organization. As of today distances (from their point of communication prevalent in plants it the view appears to be that [4] the initiation) from leaf to leaf, root to leaf would be appropriate to take a closer primary network in plants is a signal and up the stem to evoke growth look at signaling pathways involving transduction network involving responses, protein expression or Ca2+. Plants are capable of responding cytoplasmic calcium ( Ca2+) , which changes in hormone metabolism. specifically to a wide range of biotic appears to have a ubiquitous role as a There appears to be three pathways and abiotic signals. The natural cellular second messenger. This can of long distance electrical signaling in both give rise to electrical (APs & the primitive plant 'neural system' [8] : question then is , as to how the same cation (Ca2+) can be instrumental in VPs) and also interact with chemical 1) Fast moving action potentials evoking a specific response for each signals as there is evidence to suggest traveling long distances through distinct stimulus ?[11] Internal to that calcium could be an agonist or the phloem and companion cells. plant cells are mobilizable calcium antagonist for all plant growth regulators including auxin. Since Ca2+ 2) Cellular complexes in the root stores located in the vacuole, cell has limited cytoplasmic mobility , the 'transition' zone which have wall, mitochondria and endoplasmic movement of calcium within the cell 'synapses' similar to animals. reticulum (ER). On the arrival of an by means of simple diffusion is highly Despite Alpi's criticism [9] there environmental signal either calcium improbable. Rather a system of is growing evidence in the flux from external sources or release calcium channels and APTases literature that auxin can be from internal stores create transient (proteins) pump Ca2+ along specific transported from cell to cell with changes in the concentration of 2 free +
directions (relative to subcellular the aid of a calcium dependent c y t o s o l i c c a l c i u m [ C a ]2+i . compartments) resulting in vesicular trafficking system. Characteristic patterns of such [Ca ]i 'propagated waves of Ca2+ ' release [4], transients, referred to as 'calcium 3) In the case of severe trauma the amplitude and kinetics of which signatures'[11] direct downstream long distance electrical signaling are a rich source for computation and signaling events, finally leading to occurs in the xylem which is information transfer. Thus the nodes a response specific to the coupled to hydraulic pressure in this net would be Ca2+ channels and environmental stimulus. waves.
the edges probably the direction of 'Calcium signatures' are the propagating Ca2+ waves. How Apart from electrical signals, an these propagated waves of Ca2+ additional complication exists in characterized by their spatial interact with the chemical signaling plants due to plasmodesmatal location, temporal pattern and 2+
pathways is of course one of the connections between adjacent cells amplitude or strength of the [Ca ]i c e n t r a l p r o b l e m s o f p l a n t which allow the passage of proteins, transients, which confer on them the neurobiology. In any case, what is nucleic acids and other smaller ability to activate specific sets of molecules as downstream signaling being proposed is a dual molecules. Plasmodesmatal events. There is evidence that information processing system in connections are sensitive to calcium different pools of calcium stores are plants; a primary electrical system concentration, inositol phosphates, preferentially mobilized by different based on calcium signaling and a osmotic stress and probably a host of environmental cues. For example, secondary chemical system , the 61
touch and wind appear to activate the same intracellular calcium store in contrast to cold shock which largely involves extracellular Ca2+. Again highly localized regions of the cell could exhibit fluctuations in [Ca2+]i depending on the stimulus , as in the case of root hairs stimulated by the Nod factor where the increase in [Ca2+]i is in the vicinity of the 'nuclear region'.
Similar to animal cells, localized elemental events such as quarks , blips, sparks and puffs in [Ca2+]I encodes significant information relevant to the subsequent response. These localized elevations can coalesce to generate Ca2+ waves which contains encrypted information both in its amplitude and frequency. For example, in Fucus strong correlation was found between the strength of the hypo – osmotic shock and the spatio – temporal features of the [Ca2+]i waves, probably determining the response from a wide range of possibilities. One of the systems where [Ca2+]i oscillations have been extensively studied is in the stomatal guard cells, where it was found that only oscillations within a defined window of frequency, transient number, duration and amplitude resulted in steady state stomatal closure. Outside this window the oscillations led to short term Ca2+ reactive stomatal closure, a wholly different physiological response.
The calcium binding protein receptor molecules (Box 2) which perceive and can apparently differentiate calcium signatures can be divided into two classes : sensor relays and sensor responders. The former consists of the calcium binding protein calmodulin (CaM) , which then interacts with down stream Figure 1
Figure 2
62
calcineurin B like proteins (CBL). In information flow can be maintained. turn CBL's , interact with CBL - Memory and learning are thus interacting protein kinases (CIPK) , correlated. For example in the marine which directs the signal along snail Aplysia learning is due to the a p p r o p r i a t e c h a n n e l s . S e n s o r formation of new dendrites, and responders on the other hand include memory lasts as long as the specific calcium dependent protein kinases dendritic connections persist. Signal (CDPK's) which integrate both the transduction networks also have the calcium binding domain and the a b i l i t y t o d i r e c t o r i n c r e a s e kinase domain into the same information flow along specific molecule. CDPK's are again pathways either by increasing the associated with their cognate CDPK number of protein molecules or related protein kinases (CRK's) to c h a n g i n g t h e i r a f f i n i t y b y trigger specific signaling cascades. phosphorylation/ mutation. Memory There is evidence that CDPK's are results when increased signaling particularly sensitive to variation in through the specific pathway can be the calcium spikes as in the case of retained and the information is made three different CDPK isoforms in available to other interacting soybean which exhibit different pathways through cross – talk. Thus calcium thresholds for activation. at the level of networks there appears How the plant molecular machinery to be no reason why plants should be can discriminate between different incapable of learning. On the calcium signatures is a fruitful area of contrary, plants would be expected to ongoing research. display some modes of learning and seedlings with the main stem above cotyledons removed, prior exposure to either white or red light changes the pattern for bud growth. There is also considerable accumulated evidence that [Ca2+]i signatures suffer alteration by virtue of previous experience. Repeated stimulation leads to a attenuation in the amplitude of [Ca2+]i spikes and c a l ci u m s i g n at u r e s f r o m o n e environmental challenge can be modified if there has been previous exposure to a contrasting one. It is notable that Nicotiana plumbaginifolia is unable to retain the memory of cold shocks and is cold sensitive in contrast to Arabidopsis which is retentive of 'cold memory' and is also resistant to cold stress. Thus plant memory can last from a few seconds to days, weeks and months depending upon the physiological response under consideration [10]. The fairly simple paradigm to study Plant memory, learning and memory, however rudimentary.
learning involves subjecting the plant A standard practice to establish intelligence memory in plant systems is to Animals display memory, learning consider a physiological response and intelligence by virtue of their which requires two successive neural networks, which endows them environmental signals for its with plasticity in their movements initiation. By varying the time and overall behaviour. Can a similar interval between the signals, it is claim be made for plants ? In a series possible to determine the duration for of the most elegantly written articles which the memory of the first signal Trewavas [10] argues that plants are persists. Thus in the predatory plant actually intelligent organisms (not Dionaea muscipula, two successive automatons) possessed of memory action potentials have to be evoked and capable of learning. There are within 40s of each other [6] for leaf close parallels between neural nets closure and consequent entrapment and signal transduction networks. of the insect. Again tendrils require a Learning in the context of a neural net occurs when the information flux combination of mechanical stimulus rates between the signal and and blue light to coil. In this case, the adaptive response are improved by a) memory of the mechanical stimulus making new connections or b) can be retained for several hours. modifying the strength of pre- Instances have also been observed of existing connections at synaptic prior signals modifying the pattern of junctions. Memory lasts as long as the the subsequent response. For specific pathway of heightened example in de – etiolated flax to an entirely novel situation (not previously encountered in evolution) and observing its response to adapt to the altered circumstances and thereby continuing its development. It has generally been observed that exposure of plants to herbicides, initially leads to depressed growth, which the plant learns to overcome after a certain time interval. Thereafter there is accelerated growth as a compensatory measure. Thus application of Phosphon D at varying concentrations to peppermint plants, led to their diminished growth. After a few weeks the plants not only recovered their growth rate, but actually grew faster than controls. A variety of stressful situations (drought, high salt, osmotic stress, temperature extremes etc.) can be lethal to plants. However, plants can be trained under the appropriate 63
application of milder doses, to cope with the onset of more extreme conditions. behavioural intelligence systems is the capacity to predict the future : to model likely behavioural outcomes in the service of inclusive fitness.” Since plants respond primarily by growth and development rather than movement (with the exception of Mimosa and a few others) Trewavas
has modified the Learning in plants [10] can be viewed first definition in the context of plants as , “ adaptively variable growth and as a trial and error process wherein the fluctuating environmental signals development during the lifetime of the individual.” As has been mentioned are continuously processed and the previously, since the display of intelligence is an individualistic phenomenon, adaptive response optimized in averaging some physiological parameter (e.g. growth) over a large number of several iterations. In such a situation experimental specimens would not be conducive to its study. In its natural oscillatory behaviour can be expected environment plants have to grow so as to optimize its access to limited as the plant zeroes in to its optimal environmental resources (water, light, nutrients) , which is probably akin to response. Bose was one of the first to navigating a maze, a standard test for intelligent activity. Thus, plants note that petioles, leaflets and roots of continuously monitor at least 15 environmental variables with great Mimosa oscillated to its new state of precision and accuracy to yield a coordinated/integrated response. Examples growth upon exposure to novel would include the shoot sensing its nearest neighbours utilizing near – infra stimuli. Similar oscillatory red light and then taking necessary avoiding action. On the approach of behaviour was also observed in competitive neighbours the stilt palm simply moves away by differential seedling roots and shoots upon growth of prop roots supporting the stem [10]. Rhizomes (prostrate stems vertical displacement. Sustained carrying buds and roots) actively forage for new habitats which are resource oscillations were also found in rich and free from competitors. Decisions are taken as to which buds will give rhizomes upon gravitropic response. rise to leaves (instead of rhizomes) while other rhizomes continue their search. Similar to animals the learning Roots also monitor soil nutrients and take evasive action when challenged by stages appear to initially involve competitors. If intelligence involves forecasting future resource allocation for reversible modification of ion fluxes physiological action, such predictive computations are also performed by and signal transduction pathways, plants. One such example, is the dodder (Cuscuta sp.), a parasitic plant (Fig. 3) followed by gene expression for which assesses its prospective host by an initial touch contact. If found metabolic/physiological adaptation unsuitable the dodder continues its search, whereas on selection of a and finally phenotypic modification. suitable host the dodder coils around its host in a specific manner with The above changes are calibrated by resource transfer from the host commencing after several days. the sustained strength and continued presence of the environmental signal. Figure 3 A Dodder (Cuscuta sp.) coiling around its host. Finally, we come to the question of The plant does not coil around every host with which it intelligence in plants. The concept of comes into contact. Subsequent to the first contact Cuscuta asseses its prospective host before coiling intelligence (which has several levels around the host plant (Kelly, C. K. Plant foraging: a of significance) is evidently more marginal value model and coiling response in Cuscuta involved than that of either learning subinclusa. (1990) Ecology, 71, pp. 1916 – 1925 ; Kelly. C. or memory, given the difficulty K. Resource choice in Cuscuta europea. (1992) Proc. Natl. Acad. Sci. U.S.A., 89, pp. 12194 – 12197). If the inherent in its very definition. Most prospective host is found to be unsuitable the parasitic of the time there is a tendency to plant continues its search for other hosts. Photos by restrict our definition to characteristic Barry Rice, PhD;
human expressions of the faculty. http://www.sarracenia.com/galleria/galleria.html
One definition attributed to David Stenhouse [12] is, “…….adaptively variable behaviour during the By now it should be evident that modeling of information networks in plants lifetime of the individual.” Another to gain insight into its physiological activity is a task of primary importance. definition attributed to Cerra & One such attempt [13] can be found in Box 3 and Box 4. Bingham [12] is , “ The sine qua non of 64
Hopfield Model of Associative Memory
In the Hopfield model, a neuron i is represented by a two - state Ising spin at that site (i). The synaptic connections are represented by spin – spin interaction and they are taken to be symmetric. This symmetry of synaptic connections allows one to define an energy function. Synaptic connections are constructed following Hebb's rule of learning, which says that for p patterns the synaptic strength for the pair (i,j) is (1)
where i = 1,2, …….., N, denotes the ì - th pattern learned (ì = 1,2,……p). Each can take values ± 1. The parameter N is the total number of neurons, each connected in a one to all manner and p is the number of patterns to be learned. For a system of N �
neurons, each (i) with two states, (ó
�
i = 1) the energy function is (2)
The expectation is that, with wij's constructed as in (1), the Hamiltonian or the energy function (2) will ensure that any arbitrary pattern will have higher energy than those for patterns learned; they will correspond to the (local) minima in the (free) energy landscape. Any pattern then evolves following the dynamics
(3)
where hi(t) is the internal field on the neuron i, given by (4)
Here, a fixed point of dynamics or attractor is guaranteed; i.e., after a certain (finite) number of iterations t*, the network stabilizes and ói(t* + 1) = ói(t*) . Detailed analytical as well as numerical studies shows that the local minima for H in (2) indeed correspond to the patterns (with 100 % overlap) fed to be learned in the limit when memory loading factor á = (p/N) tends to zero; and they are less than ~3% off from the patterns (97 % overlap) fed to be learned when á < ác ~ 0.14. Above this loading, the network goes to a confused state where the local minima in the energy landscape do not have any significant overlap with the patterns fed to, or learned by, the network.
[ For details see Hertz,J., Krough, A. and R.G. Palmer, R. G. Introduction of Theory of Neural Computation. Addison-Wesley Publishing, Cambridge, MA (1991) ]
Summing up To sum up [14], Bose's primary intuition of plants as living organisms capable of intelligent behaviour ( a property of the whole organism) stands in the process of being completely justified. Progressively, there seems to be little doubt that aspects of intelligent behaviour, such as memory, learning, decision – making, sensing, predictive foresight to optimize 'resource acquisition with economy of effort' are found in varying degrees in plants. Some could even possess all these intelligent capabilities. It is somewhat ironic that current developments in botany had been foreseen by Bose about a hundred years ago, though they were consistently rejected during his lifetime. The entire matter is put in a nutshell by Brenner et al [8], “ Bose's overall conclusion that plants have an electro – mechanical pulse, a nervous system, a form of intelligence, and are capable of remembering and learning, was not well received in his time A hundred years later, concepts of plant intelligence, learning and long – distance electrical signaling in plants have entered mainstream literature.”
65
A Hopfield – like Plant Intelligence Model
Let us first briefly mention several results concerning properties of the plant units (cells), namely, the current (I) – voltage (V) characteristics of their cell membrane. In Fig.1 [(a) The non-linear current (I)-voltage (V ) characteristics of cell membranes. (b) Its Zener diode like representation with threshold voltages indicated by VT ], we show the typical non – linear I – V characteristics of cell membranes acting as logical gates [See Chakrabarti, B. K. and Dutta, O. An electrical network model of plant intelligence. Ind. J. Phys. A 77, pp. 551-556 (2003) ] From this figure , we find that the I – V characteristics are equivalent to those of the Zenner Diode. Namely, some threshold vT exists crossing which, the direction of the current changes. By assuming that the current has two directions, that is ± 1, and the voltage is determined by the weighted contributions, Chakrabarti and Dutta (2003) constructed a mathematical plant cell as a non – linear unit. From the viewpoint of input – output logical units like perceptrons for neural networks, the output of the i – th unit Oi is given by where strength of each connection wij is all positive or negative. Note that in the Hopfield model it is given as ± randomly distributed weight matrix in terms of the Hebbian rule From these experimental results and simple observations, we now ask a natural question: could the plants act as memory devices similar to a real brain ? Obviously, in the above model of a plant network, there is no frustration in the network as in animal brain models [Inoue, J. and Chakrabarti, B. K. Competition between ferro-retrieval and antiferro orders in Hopfield-like network model plant intelligence. Physica A , 346, pp. 58-67 (2004) ]. The above mentioned paper attempts to elucidate, as to what extent constraints on the sign of the weight matrix influences the ability in plants to retrieve patterns as associative memories.
For this purpose, they introduce a simple plant intelligence model based on a Hopfield - like model in which ferromagnetic retrieval and anti – ferromagnetic ordered phases co exist. Inoue & Chakrabarti (2004) start from the following Hamiltoni an
where we defined the following two parts of the total Hamiltoni an As in Box 3, the vector æì = { æì1 ………. æìN} denotes the ì – th embedded pattern and ó = {ó1…….., óN} stands for neuronal states. A single parameter �
�
��
, the system determines the strength of the antiferromagnetic order. That is to say, in the limit of �
is completely determined by the energy function HAF. On the other hand, in the limit of �
�
�0, the system becomes identical to the conventional Hopfield model. Comparing with the Hopfield model results as in Box 3, it was shown by Inoue & Chakrabarti (2004) that the memory capacity of this plant network model decreases considerably with �
, leaving the network with a weak memory capacity [ For review see Inoue, J. A simple Hopfield-like cellular network model of plant intelligence in Ref. 13, pp. 169-174 ] 66
Gubb, I. R., Reilly, A. J., Skipper, Y. Aspects of plant intelligence. D., Doherty, H. M., O,Donnell, P. (2003) Annals of botany, 92 , pp. 1- This article has been developed from J. and Bowles, D. J. Electrical 20 ; Trewavas, A. Mindless a previous article published in signaling and systemic mastery (2002) Nature, 415, pp. Science & Culture, Vol 74 (11-12) proteinase inhibitor induction in 841.
Nov-Dec (2008) pp.423-432. Mr. the wounded plant. (1992) Nature, 11. McAinsh, M. R. & Pittman. J. K. Kausik Das and Mr. Venugopal are 360, pp. 62 – 65; 17. Simons, P. J. Shaping the calcium signature acknowledged for technical The role of electricity in plant (2009) New Phytologist , 181, pp. assistance. movements. (1981) New Phytol. 275 – 294; Bose, I. & Karmakar, R., 87, pp. 11 – 37.
References
Simple Models of Plant Learning and Memory. (2003) Physica 1. Bose, J. C. The nervous 7. Bothwell, J. H. F. & Ng, C. K. –Y . Scripta, Vol. T106, pp. 9-12. The evolution of Ca2+ signaling in mechanism of plants, Longmans, photosynthetic eukaryotes. London (1923) 12. Stenhouse, D. The evolution of (2005) New Phytol., 166, pp. 21 – intelligence – A general theory 2. Bose, J. C. Action of drugs in 38.
and some of its implications. plants (1914) Proc. R. Soc. Med. 8, (1974) George Allen & Unwin ; 8.
Brenner, E. D., Stahlberg, R., pp. 1 – 40.
La Cerra & Bingham, R. The Mancusco, S., Vivaanio, J., 3. Bose, J. C. The high magnification origin of minds. (2002) Harmony Baluska, F. & Van Volkenburgh, crescograph for researches on Books, New York.
E. Plant neurobiology : an growth. (1918) Trans. Bose Res. i n t e g r a t e d v i e w o f p l a n t 13. Banerjee, R. & Chakrabarti, B. Inst. 1, pp. 151 – 172.
signaling. (2006) Trends in plant K.(Eds.) Models of Brain and Mind: 4. Shepherd, V. A. From semi – science, 11(8), pp. 413 – 419 ; Physical, Computational and conductors to the rhythms of Barlow, P. W. Reflections on 'plant Psychological Approaches, (2008), sensitive plants : The research of neurobiology'. (2008) Biosystems, Progress in Brain Research 168, J. C. Bose. (2005) Cell & Mol. Biol. 92, pp. 132 – 147; Brenner, E. D., Elsevier , Amsterdam, pp. 1-266.
51, pp. 607 – 619.
Stahlberg, R., Mancusco, S., Baluska, F. and Van Volkenburgh, 14. For extensive bibliography we 5. Batiza, A. F., Schulz, T. & Masson, refer to Chakrabarti, B. K., Inoue, E. Response to Alpi et al. : Plant P. H. Yeast respond to hypotonic J. I. and Banerjee, R., Learning, neurobiology the gain is more shock with a calcium pulse. (1996) memory & intelligence in plants; than the name. (2007) Trends in J. Biol. Chem. 271, pp. 23357 – insights of Acharya J. C. Bose : plant science, 12(7), pp. 231 – 233.
23362.
then & now. (2008) Science & 6. Fromm, J. & Lautner, S. Electrical 9. Alpi et al. Plant neurobiology : no Culture, Vol. 74 (11-12) Nov-Dec, brain, no gain. (2007) Trends in signals and their physiological pp. 423-432.
plant science, 12(4), pp. 135 – 136.
significance in plants. (2007) Plant, Cell and Environment, 30, 10. Trewavas, A. Response to Alpi et pp. 249 – 257 ; Wildon, D. C. , al. (2007) Trends in plant science, Thain, J. F., Minchin, P. E. F., 12(6), pp. 231 – 233 ; Trewavas, A. Acknowledgment
67