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ScienceDirect Journal homepage: www.elsevier.com/locate/cortex

Special section: Editorial

A plastic brain for a changing environment Costanza Papagno a,* and Giuseppe Vallar a,b a b

Department of Psychology, University of Milano-Bicocca, Piazza dell'Ateneo Nuovo 1, 20126 Milano, Italy Neuropsychological Laboratory, IRCCS Istituto Auxologico Italiano, Milano, Italy

A few years ago a brief communication on Nature reported learning-induced plasticity in the gray matter of the brains of volunteers who had learned to juggle (Draganski et al., 2004). These individuals showed a transient and selective structural change in brain areas associated with the processing and storage of complex visual motion. This discovery of a stimulus-dependent alteration in the brain's macroscopic structure contradicted the traditional, and at that time prevailing, view that cortical plasticity is associated with functional, rather than anatomical, changes (Draganski & May, 2008). This finding gave also impetus to the study of neuroplasticity, suggesting that in the gray matter not only reduction of volume is possible, such as in ageing, but also increment. There may be, however, some abuse of the term “neuroplasticity” (used with “gay abandon”, as suggested by Buchtel, 1978). Following Paillard (see Will, Dalrymple-Alford, Wolff, & Cassel, 2008), changes in the nervous system should be called “plastic” only when the connectivity network of the system undergoes lasting changes in the structure that links together its elements. Furthermore, changes, to be considered “plastic”, should be both structural and functional, namely only when a given system (here, a set of cortico-subcortical networks) achieves a novel function, either by transforming its pattern of internal connectivity, or by changing the elements of which it is made, or both. Random (background noise) and systematic variations, namely, operating errors beyond the flexibility of the system, as well as vicarious strategies used to achieve a given behavioral goal should not be regarded as plastic changes. With reference to the life span of the living organism, the distinction may be drawn between the structural malleability of the system during development, within the range of genetic competence (termed by Paillard genetic plasticity), and the capacity of the fully developed system to change its own structure, and to expand its behavioral repertoire, namely: the adaptive plasticity of a system which

has already completed its maturation. The possibility that a given neural system achieves a novel function does not necessarily mean that the functional (psychological, cognitive) architecture changes. The function may be “novel”, with reference to the previous activity of that neural network, but not per se, namely: the plastic system may replace, at least in part, another damaged network, taking over and maintaining the functional properties of the latter. This is a key assumption, in order to make meaningful inferences from the pathological behavior of brain-damaged patients to the functional organization of the normal system (discussion in Vallar, 2000). Finally, plasticity refers to a change in structure in response to an external force, and the maintenance of that shape after removal of the force, in contrast to “elasticity”, which implies the return to the previous form, when the force is removed (Berlucchi & Buchtel, 2009). While convincing empirical evidence suggesting that plastic changes may occur in the brain is quite recent, the roots of the concept of “neuroplasticity” may be traced back to the second half of the XIX century. Berlucchi and Buchtel (2009) pointed out that the Italian psychiatrist Ernesto Lugaro (1870e1940) was the first to introduce the term “plasticity” (also used by the North American psychologist William James, to denote changes in nervous paths associated with the establishment of habits) in order to link neuroplasticity to synaptic plasticity as early as 1906. By this term Lugaro meant that the anatomoefunctional relations between neurons might change in an adaptive way along our life span, in order to allow psychic maturation, learning, as well as functional recovery after brain damage. Lugaro's concept of plasticity was inspired by a neural hypothesis of learning and memory put forward in 1893 by his mentor Eugenio Tanzi, who postulated that practice and experience promote neuronal growth and identified the articulation between neurons as sites of neural plasticity. Cajal (references in Berlucchi &

* Corresponding author. Department of Psychology, University of Milano-Bicocca, Piazza dell’Ateneo Nuovo 1, 20126 Milano, Italy. E-mail addresses: [email protected], [email protected] (C. Papagno), [email protected] (G. Vallar). http://dx.doi.org/10.1016/j.cortex.2014.06.001 0010-9452/© 2014 Elsevier Ltd. All rights reserved.

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Buchtel, 2009) refined Tanzi's hypothesis with his own idea of plasticity as the result of the formation of new connections between cortical neurons. After a period of decadence, also due to the diffusion of Lashley's views (1938) of a functional equipotentiality of the cortex e so that novel functions in a neural system can not emerge, due to plastic changes e neuroplasticity flourished again with Donald Hebb (1949). Currently, research interest in these issues has received new impulse under the growing evidence in favor of the existence of a considerable degree of plasticity even in the mature and aged brain, which constitutes a neural basis for neurological and neuropsychological rehabilitation after brain damage (Berlucchi, 2011). Most information on neuroplasticity has been achieved by means of experiments in laboratory animals (Kolb & Gibb, 2014; this Special Section). More recently, these have been complemented with non-invasive brain stimulation (NIBS) techniques (Transcranial Magnetic Stimulation, TMS; transcranial Electrical Stimulation, tES). NIBS modulates sensorimotor performance and higher-level behavior in both neurologically unimpaired participants and brain-damaged patients (Miniussi & Vallar, 2011); they are capable of inducing shortlasting changes in the human cortex (Vallence & Ridding, 2014; this Special Section), and simulate changes occurring in brain damage (Cattaneo et al., 2014; this Special Section). Whether these short-lasting changes fulfill Paillard's criteria for “plasticity” is not clear. Probably, they are, in a much broader sense. It is likely to be the case that plastic modifications, as qualified above, may be variably lasting in time, and their duration likely to be dependent on many factors, including the type, the duration and the temporal organization of the plasticity-inducing experience. Another possible difference between current views about plasticity and Paillard's original suggestion, is that experience (including NIBS) may potentiate the activity of a neural network (with long lasting structural and functional changes) without modifying its overall functional properties. Overall, the main criteria for plasticity appear to be the occurrence of structural and functional changes, related to experience. Experience modifies internal representations in the brain, as in procedural learning (Censor, Dayan, & Cohen, 2014; this Special Section); this phenomenon is not unique to sensory and motor systems, but also applies to cognitive functions. An example of cognitive plasticity is offered by the study by Takahashi et al. (2014, this Special Section), who show that different impressions obtained through social interaction with a variety of agents uniquely modulate the activity of dorsal and ventral pathways of the brain network that mediates human social behavior. Changes occurring in polyglots' brain provide another example of plasticity. This is crucial now that we are living in a multilingual society. How does neuroplasticity occur in the brain as a function of an individual's experience with a second language? It is not until recently that we have gained some understanding of this question, by examining the anatomical changes, as well as the functional neural patterns induced by the learning and use of multiple languages (review by Li, Legault, & Litcofsky, 2014; this Special Section). However, although there is somewhat of a natural tendency to think of plasticity as a positive influence on brain

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organization, there are many examples of negative effects of plasticity on brain and behavior, such as the phantom limb € der, 2011). experience (Nava & Ro In the same individual, positive and negative effects of plasticity can appear. One example comes from the study of deaf population. Losing one type of sensory information at specific developmental times, may lead to deficits across all sensory perception, demonstrating that plasticity does not necessarily result in behavioral compensation. Compared with hearing people, deaf individuals are impaired in tactile temporal processing, suggesting that early hearing experience is crucial to develop an efficient temporal processing across modalities (Bolognini et al., 2012). Auditory deprivation (irrespective of sign language experience) affects also the typical pattern of hemispheric asymmetry in spatial attention, which reflects the dominance of the right hemisphere in neurologically unimpaired participants (Cattaneo, Fantino, Mancini, Mattioli, & Vallar, 2012; Jewell & McCourt, 2000), as measured through a visual line bisection task, in which a leftward bias (“pseudoneglect”) is observed. The lack of a significant directional bias, with no decrement of accuracy, in the deaf seems to suggest that the two hemispheres may be more equally involved in controlling spatial attention, providing in the same type of individuals an example of plasticity, “positive” in that it does not hinder the function (Cattaneo, Lega, Cecchetto, & Papagno, 2014). Finally, current research has also outlined the role that the white matter plays in neuroplasticity, in addition to that of the cortex. Not only this is evident for motor and sensory deficits, where the lack of recovery in patients with extensive subcortical damage is a consistent finding (Heiss & Kidwell, 2014; Lindenberg & Seitz, 2012), but also cognitive performance requires participation of white matter fiber tracts (Duffau, 2014; this Special Section). Naming famous people is definitely impaired when a white matter tract is removed (Papagno, Miracapillo, et al., 2011). Studies with direct electrical stimulation have underlined the crucial role of subcortical connections in shaping the cortical reorganization of the networks involved in object naming following perturbation of normal function due to slowly evolving brain damage, such as a tumor (Papagno, Gallucci, et al., 2011). In humans, neuroplastic modifications play a main role in the persons' ability to cope successfully with both environmental and internal (e.g., a disease) changes. Nevertheless, maladaptive plastic changes may occur also in response to a variety of pathological conditions, as we have mentioned. This Special Issue considers some aspects of “neuroplasticity”, used in its broadest sense, from both a behavioral and a neural perspective: it includes contributions (reviews and empirical studies) concerning motor, perceptual and cognitive plasticity, and their neural underpinnings, in both healthy participants and patients with brain damage and dysfunction.

references

Berlucchi, G. (2011). Brain plasticity and cognitive neurorehabilitation. Neuropsychological Rehabilitation, 21(5), 560e578.

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Berlucchi, G., & Buchtel, H. A. (2009). Neuronal plasticity: Historical roots and evolution of meaning. Experimental Brain Research, 192(3), 307e319. Bolognini, N., Cecchetto, C., Geraci, C., Maravita, A., PascualLeone, A., & Papagno, C. (2012). Hearing shapes our perception of time: temporal discrimination of tactile stimuli in deaf people. Journal of Cognitive Neuroscience, 24(2), 276e286. Buchtel, H. A. (1978). On defining neural plasticity. Archivio Italiano Di Biologia, 116(3e4), 241e247. Cattaneo, Z., Fantino, M., Mancini, F., Mattioli, F., & Vallar, G. (2012). Listening to numbers affects visual and haptic bisection in healthy individuals and neglect patients. Neuropsychologia, 50(5), 913e925. Cattaneo, Z., Lega, C., Cecchetto, C., & Papagno, C. (2014). Auditory deprivation affects biases of visuospatial attention as measured by line bisection. Experimental Brain Research, 1e7. http://dx.doi.org/10.1007/s00221-014-3960-7 [Epub Ahead of Print]. Cattaneo, Z., Renzi, C., Casali, S., Silvanto, J., Vecchi, T., Papagno, C., et al. (2014). Cerebellar vermis plays a causal role in visual motion discrimination. Cortex, 58, 272e280. Censor, N., Dayan, E., & Cohen, L. G. (2014). Cortico-subcortical neuronal circuitry associated with reconsolidation of human procedural memories. Cortex, 58, 281e288. Draganski, B., Gaser, C., Busch, V., Schuierer, G., Bogdahn, U., & May, A. (2004). Neuroplasticity: changes in grey matter induced by training. Nature, 427(6972), 311e312. Draganski, B., & May, A. (2008). Training-induced structural changes in the adult human brain. Behavioural Brain Research, 192(1), 137e142. Duffau, H. (2014). The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex, 58, 325e337. Hebb, D. O. (1949). The organization of behavior. New York: John Wiley. Heiss, W.-D., & Kidwell, C. S. (2014). Imaging for prediction of functional outcome and assessment of recovery in ischemic stroke. Stroke, 45(4), 1195e1201. Jewell, G., & McCourt, M. E. (2000). Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks. Neuropsychologia, 38(1), 93e110. Kolb, B., & Gibb, R. (2014). Searching for principles of brain plasticity and behavior. Cortex, 58, 251e260.

Lashley, K. S. (1938). Experimental analysis of instinctive behavior. Psychological Review, 45(6), 445e471. Li, P., Legault, J., & Litcofsky, K. (2014). Neuroplasticity as a function of second language learning: anatomical changes in the human brain. Cortex, 58, 301e324. Lindenberg, R., & Seitz, R. J. (2012). Impact of white matter damage after stroke. In P. Bright (Ed.), Neuroimaging e Methods (pp. 233e244). Rijeka, Croatia: InTech Europe. Miniussi, C., & Vallar, G. (Eds.). (2011). Special issue: non-invasive brain stimulation: new prospects in cognitive neurorehabilitation. Neuropsychological Rehabilitation, 21, 553e768. € der, B. (2011). Adaptation and maladaptation. Nava, E., & Ro Insights from brain plasticity. Progress in Brain Research, 191, 177e194. Papagno, C., Gallucci, M., Casarotti, A., Castellano, A., Falini, A., Fava, E., & Caramazza, A. (2011). Connectivity constraints on cortical reorganization of neural circuits involved in object naming. NeuroImage, 55(3), 1306e1313. Papagno, C., Miracapillo, C., Casarotti, A., Romero Lauro, L. J., Castellano, A., Falini, A., & Bello, L. (2011). What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain, 134(2), 405e414. Takahashi, H., Terada, K., Morita, T., Suzuki, S., Haji, T., Kozima, H., & Naito, E. (2014). Different impressions of other agents obtained through social interaction uniquely modulate dorsal and ventral pathway activities in the social human brain. Cortex, 58, 289e300. Vallar, G. (2000). The methodological foundations of human neuropsychology: studies in brain-damaged patients. In F. Boller, J. Grafman, & G. Rizzolatti (Eds.), Handbook of neuropsychology (2nd ed.), (Vol. 1); (pp. 305e344). Amsterdam: Elsevier. Vallence, A.-R., & Ridding, M. (2014). Non-invasive induction of plasticity in the human cortex: uses and limitations. Cortex, 58, 261e271. Will, B., Dalrymple-Alford, J., Wolff, M., & Cassel, J.-C. (2008). Reflections on the use of the concept of plasticity in neurobiology. Translation and adaptation by Bruno Will, John Dalraymple-Alford, Mathieu Wolff and Jean-Christophe Cassel from J. Paillard, J Psychol 1976;1:33e47. Behavioural Brain Research, 192(1), 7e11.

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