Motor learning processes: an electrophysiologic perspective

Processos de aprendizagem motora: uma perspectiva eletrofisiológica

ARTICLES

Motor learning processes: an electrophysiologic perspective

Processos de aprendizagem motora: uma perspectiva eletrofisiológica

Bruna Velasques^{I, VI}; Camila Ferreira^I; Silmar Silva Teixeira^V; Vernon Furtado^V; Elizabeth Mendes^V; Luis Basile^II; Mauricio Cagy^{I, IV, V}; Roberto Piedade^{I, VI}; Pedro Ribeiro^{I, III, IV, V, VI}

^ILaboratório de Mapeamento Cerebral e Integração Sensório-Motora, Programa de Pós-Graduação em Psiquiatria e Saúde Mental (PROPSAM), Instituto de Psiquiatria da Universidade do Brasil (IPUB), Universidade Federal do Rio de Janeiro, Brasil (UFRJ)

^IIDivisão de Neurocirurgia Funcional, Instituto de Psiquiatria, Escola de Medicina, Universidade de São Paulo, Brasil (USP)

^IIIDepartamento de Biociências da Atividade Física, Escola de Educação Física e Desportos (EEFD), UFRJ, Brasil

^IVDepartamento de Epidemiologia e Bioestatística, Instituto de Saúde da Comunidade, Universidade Federal Fluminense, Rio de Janeiro, Brasil (UFF)

^VPrograma de Pós-Graduação Strictu Sensu em Ciência da Motricidade Humana (PROCIMH), Universidade Castelo Branco, Rio de Janeiro, Brasil

^VIInstituto Brasileiro de Biociências Neurais (IBBN), Rio de Janeiro, Brasil

ABSTRACT

The goal of the present study was to investigate electrophysiologic, qEEG, changes when individuals were exposed to a motor task. Subjects’ brain electrical activity was analyzed before and after the typewriting training task. For the neurophysiological variable asymmetry, a paired t-test was performed to compare each moment, pre and post-task, in the beta bands. The findings showed a change for the qEEG variable in each scalp site, F₃/F₄; C₃/C₄ and P₃/P₄. These results suggest an adaptation of pre-frontal, sensory-motor and parietal cortex, as a consequence of the typewriting training.

Keywords: sensory-motor integration, procedural learning, qEEG.

RESUMO

O objetivo do presente estudo foi investigar mudanças eletrofisiológicas através do EEGq quando indivíduos são expostos a uma tarefa motora. A atividade elétrica no córtex dos sujeitos foi analisada antes e após o treinamento da tarefa motora. Para a variável neurofisiológica assimetria, um teste t foi implementado para comparar cada momento, pré e pós-tarefa, na banda beta. Os achados demonstraram mudança em assimetria para as seguintes regiões no escalpo: F₃/F₄, C₃/C₄ e P₃/P₄. Estes resultados sugerem uma adaptação das regiões pré-frontal, somatosensorial e parietal como conseqüência do treinamento de datilografia.

Palavras-chave: integração sensório-motora, memória de procedimento, EEGq.

To maintain stability at a highly dynamic environment, the central nervous system (CNS) is in constant activity. It continuously receives external sensory stimuli, many specifically required to maintain motor performance^1-3. Many studies have demonstrated that precision during the motor gesture is increased as consequence of motor learning^4,5. Motor learning promotes a gradual minimization of task errors, an increase in coordination, agility and movement execution⁶.

Different mechanisms take part in the complexity of motor learning which involves various levels of cortical structures, such as: pre frontal areas related to decision making, contralateral primary motor cortex⁷, ipsilateral primary motor cortex, supplementary motor area, pre motor area, primary sensory areas⁸, and the parietal region responsible for information integration processes. The different functional components and the plastic reorganization of the CNS have lead to investigations objecting the examination of neurofunctional phenomena involving motor learning⁹.

Hence, this study aimed at investigating how participative is the learning of a motor task in the cortex organizational mapping. For that, we used quantitative electroencephalography (qEEG) to detect neural changes during the motor learning process¹⁰. Beta activity was specifically investigated, since it is responsive to movements and electro-stimulation of limbs^11,12.

METHOD

The methodology was presented before by our group in several other studies^13-15. Thus, the methods will be summarized below.

The sample was composed for 29 healthy individuals, both sexes, with ages varying between 20 to 40 years, absence of mental and physical illness (previous anamnese), right handed (Edinburgh)¹⁶, and do not making use of any psychoactive or psychotropic substance during the whole time of the study. The experiment consisted of a task of a typewriting method of progressive learning, in which training was performed on a single day. The exercise was made up of four blocks, each block represented by twelve lines. Each line had five sequences of letters for each hand.

Spatial electrode localization and frequency bands – Three areas of interest were investigated: pre frontal, central and parietal. Pre frontal area is related to motivation, planning and decision making. Central area is associated with sensory reports of motor gesture and execution of voluntary movements, corresponding to the somatosensory and primary motor cortex. The parietal region, including the posterior-parietal cortex relates to sensory and attention integration processes. The beta band (13–25 Hz) was than selected due to its relation to somatomotor processes.

Statistical analysis – As electrodes have different scalp (spatial) positions, we have chosen an independent statistical analysis. A t-test was employed for each electrode at beta (F₃-F₄/C₃-C₄/P₃-P₄).

RESULTS

Neurophysiological variables – Figure1 describes the variation in asymmetry between pre and post training times at F₃/F₄. Statistical analysis has demonstrated a significant difference between two experimental times (p=0.003).

Figure 2 displays the variation in asymmetry between the pre and post training times at C₃/C₄, with a significant difference of (p=0.019).

Figure 3 represents the oscillation in asymmetry between pre and post training times P₃/P₄. Statistical difference was also significant (p=0.025).

DISCUSSION

This investigation aimed at examining electrophysiological alterations produced by a learning task through quantitative electroencephalography. The discussion will be presented following the results appearance. Hence, the first section elaborates on the participation of the prefrontal cortex in planning and decision making processes. The second section conjectures over the possible plastic alterations occurring in the somatosensory cortex as a consequence of the motor task. The third section focus on the electroencephalographic outcomes regarding changes in the parietal cortex.

Prefrontal cortex: memory and planning – The prefrontal cortex is responsible for anticipation of consequences, planning and organizing strategies^17,18. Our results show an increased hemispheric asymmetry at prefrontal regions following the two-hour typewriting task. Since all individuals had a prior experience with typewriting, it was assumed that they were all at the so-called "controlled stage" of learning¹⁹. This stage is associated to initial periods of learning where subjects divide the attention focus with differentiated elements of the task and the environment², leading to reduced motor coordination, increased number of mistakes and execution time. As observed in the results, such increase in symmetry suggests changes in the representation of neuronal activity at the prefrontal cortex, as noticed by other investigations^18,20. The prefrontal cortex integrates with the limbic associative cortex, connecting directly to limbic structures as the amigdala and the cingulate cortex. Therefore, the results imply changes in structures associated with procedural memory, in particular the way information is registered^21,22.

Somatosensory cortex: plastic alterations as a consequence of the task – Results demonstrate that the two-hour typewriting training produced asymmetry changes at C₃/C₄, suggesting a reorganization of neuronal activity at the somatosensory cortex. Previous studies have observed such alterations as a consequence of sequential repeated finger movements^23,24. It is important to remind that these investigations used animals and that they trained for months. Experimental proportions must be considered since training mode in primates (monkeys) is different from humans and gesture specificity between species is a key factor in cortical representation²⁵. The reason between cortical areas, as expressed in asymmetry (C₃/C₄), detects changes in the relation between the two hemispheres after the typewriting task. This allegedly means that increased symmetry between regions suggests a reorganization of the supposed interaction between the two hemispheres¹³. It is essential, however, to replicate these findings employing other neuroimaging techniques since the spatial resolution of EEG does not allow a precise cortical identification of hands and fingers.

Posterior parietal cortex: attention and sensory integration processes – Our results show reduced asymmetry at P₃/P₄. Beta activity is related to stimulation processes and voluntary movements^26,27. Posterior parietal cortex (Brodmann areas 5 and 7) is located next to the somatosensory primary area (S-1) and possesses neurons with great receptive fields, which allows this region to specialize in differentiated and complex activities. The parietal cortex has a convergence site of simple and segregated sensory stimuli, functioning as a multiple integration organization^28,29. Therefore, the parietal region is associated to visual and motor information, also waking and attention mechanisms as well³⁰. The reduced asymmetry values suggest possible changes in somatosensory and visual integration processes. Particularly, neurons in the area 5 collect information from different articulations or arm muscle groups; and neurons in the area 7 integrate tactile and visual stimuli, and participate actively in the eye-hand coordination³¹. The posterior parietal cortex also receives visual communication regarding the representation of the visual world and movement planning. Consequently, such variation in asymmetry might represent a task automaticity process³².

Received 16 January 2007, received in final form 6 June 2007. Accepted 6 August 2007.

Dra. Bruna Brandão Velasques - Rua Paula Brito 350 / 1102 - 20541-190 Rio de Janeiro RJ - Brasil. E-mail: [e-mail]

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Publication Dates

• Publication in this collection
  06 Dec 2007
• Date of issue
  Dec 2007

History

• Reviewed
  06 June 2007
• Received
  16 Jan 2007
• Accepted
  06 Aug 2007