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Brain Lateralization

?

General Questions

General Questions

1. Why do humans developed a contralateral movement control?

2. Why and when do human expressed hand dominance (handedness)?

3. Why do changes in mobility alter the contralateral control?

Contralateral control hypotheses

Contralateral Hypotheses

1. Avoidance behavior hypothesis (Cajal RY 1899)

2. Image-forming eye hypothesis (Sarnat HB, Netsky M, 1976)

3. Binocularity hypothesis (Serge et al., 2005)

4. Bilaterality hypothesis (Polyak 1957)

5. Mobility hypothesis (Whitehead and Banihani 2017):

  • Mobility enables animals to avoid predators and to reach locations that are more conducive to survival.
  • Mobility also enables an animal to find food, water and suitable mates. For all these reasons there would be a significant evolutionary advantage favoring the development of anatomical features that lessen the chance of losing mobility.
  • Contralateral control could provide such an advantage.

Mathematically modeling the dependence of mobility impairment

How?

Wellness equation (functionality of the system after injury)

n = Fixed number greater than one indicating degree of non-linearity

f = Destruction fraction between 0 and 1

W= Represents the functionality of the system after injury or "wellness".

Probability of survival equation

Given a W of 0.8 the probability of survival will be P= 67%

When left and right hemisphere are included in the equation ( computing 1,000 trials)

Over a random sampling of these scenarios, contralateral control provides a survival advantage of 5% higher than ipsilateral control.

Handedness hypothesis

Why?

Sainburg World

To accommodate increasingly complex and coordinated behaviors (i.e., bimanual activities) during the course of evolution required the development of a more extensive neural circuits to carry out the underlying computations.

Option 1: Expanding brain size (too be costly in terms of energy and distance).

Option 2: Specialization of neural circuits within one hemisphere in order to develop more efficient local circuits. Yes!

Motor lateralization identifies two different computational processes associated with voluntary motor control:

1) Left Hemisphere: Predictive control that specifies trajectories and accounts for initiation movement dynamics including energetics

2) Right Hemisphere: Impedance control that specifies velocity and final position accuracy as well as robustness against unpredictable perturbations. It is feedback-dependent to correct ongoing movements.

The Invariant Lateralization Theory

Kinsbourne (1975) and Witelson (1987)

When?

Developed as a response of the Progressive Lateralization Theory of Lenneberg (1967) suggesting that there is a critical period for language acquisition and as such, hemispheric specialization of function for language occurs during that same period of development. Since hemispheric specialization for language is highly related to specialization for handedness (Knecht, et al. 2000).

The Invariat Lateralization Theory suggest that head turning can be seen as a precursor of locomotion toward one side. There is a relationship between the direction of the most frequent head turning in the infant and subsequent hand preference. At the intrauterine age of 32 weeks (Turkewitz, 1977) showed that there is asymmetric tonic neck response.

Kinsbourne (1970) proposed that a motor bias that in most individuals is targeted rightward clearly exists as early as at birth or even before and is a major determinant of the side of the subsequently preferred hand. Contrary to the assumption that handedness emerges from diffuse movement patterns in infancy.

Mobility Disruptor

Mobility driven

motor adaptations

1. Insults to the Central Nervousness System (CNS): Stroke, cerebral palsy, hemispherectomy, etc.

2. Limb Immobilization: Surgical interventions, trauma to the soft and skeletal system, forced limb immobilization, pain, spinal cord injury, etc.

3. Congenital and acquired limb deficiency: Traumatic limb loss, surgical interventions, congenital reduction deficiencies, amniotic band syndrome, malformations, etc.

If mobility is the driving force for neural adaptations, then how humans adapt to the congenital absence of a limb?

Specific Questions

1. Does contralateral control remains?

2. What is the role of the non-affected hand?

3. How do children adapt to a prosthesis?

Proposition:

Children with congenital unilateral upper-limb reductions may lack representation of the missing part of the limb in the cerebral cortex. As a consequence, the child may have a limited number of “motor repertoires” for the affected upper-limb.

Can this be related to the upper-limb prosthesis high rejection rate?

Theoretical Framework

Theoretical Support:

  • Dynamic systems theory (Thelen E, & Smith 1994)
  • Developmental systems approach (Gottlieb 2007) Dynamic field theory (Wiebee et al., 2014)
  • Interactive specialization (Johnson 2011)
  • Neural Group Selection Theory (Sporns and Edelman 1993).

Neural Group Selection Theory

NGST

  • Under this framework, NGST suggests that intervention in these children at an early age, such as prosthetic fitting and use, may lead to an enlargement of the primary neuronal networks located in the cortical area involved with motor control of the affected limb.

  • Ultimately, this may lead to a larger repertoire of motor strategies and integration of the prosthesis into the sensory and motor control of the child, facilitating prosthesis acceptance (Hadders-Algra group, Nehterlands).

  • However, there is a lack of evidence supporting this hypothesis in pediatric populations. Furthermore, there exists no quantitative evidence suggesting that wearing a prosthesis has any influence on the primary motor cortex of children with congenital upper-limb reductions or if this influence is reflected in changes in motor performance.

Normal Development

Mechanism of Action

  • Developmental Selection (form the innate primary neural repertoire)
  • Experiential Selection (from experiences)
  • Reentry: Recursive(repeated) process of changing synaptic strength in different parts of the brain.

Experimental Design

Methods

An experimental group of children with unilateral upper-limb reduction deficiency on the left side. A sex- and age matched control group performed a gross manual dexterity task with the preferred (right) and non-preferred (left) sides while measuring motor cortical activity in both hemispheres.

The experimental group performed the motor task wearing a prosthesis on the non-preferred side (affected left side) and similarly, the control group performed the same task wearing a prosthetic simulator on the non-preferred side (also left side).

All children (experimental and control groups) showed right-hand preference.

fNIRS

  • A continuous wave 24-channel fNIRS system (Hitachi ETG-4000, Hitachi Medical Corporation, Tokyo, Japan)

  • The headgear was positioned over the C3 and C4 landmarks

  • The NIRS Brain AnalyzIR Toolbox40 was used to analyze the fNIRS data (General Linear Model).

  • The GLM model is described by the equation Δ [Hbx]=X∙β+ ε , where delta[Hbx] represents the measurement vector (HbO, HbR, or HbT), while X stores information regarding event onset and termination including the design matrix encoding the timing of stimulus events, B defines the unknowns in the model representing the weighted regression coefficients for a particular source-detector channel. and E represents measurement error.

Functional near-infrared spectroscopy (fNIRs)

Hypothesis

It was hypothesized that:

i) Dexterity will not be significantly different between prosthesis and simulator groups.

ii) lateralization of the brain will be less pronounced for prosthesis users (due to less specialized neural organization).

Results

Results

TD Right Hand Task

TD Left Hand Task

Cortical Activation

Cortical Activation & Brain Lateralization

  • The typically develop (TD) group presented preferential activation in the contralateral motor cortex while performing the motor task.

  • In contrast, the children with ULD showed preferential activation in the ipsilateral motor cortex when using the non-preferred side (affected side with prosthesis).

  • Thus, the ULD group was found to have significant ipsilateral dominance for the non-preferred hand with the prosthesis when compared to the TD group using the simulator

ULD Right Hand Task

ULD Left Hand Task

Major Findings

Discussion and Conclusion

The major findings of the present investigation are in agreement with our hypotheses indicating

  • A non-significant difference in gross manual dexterity between prosthetic and prosthetic simulator groups

  • Children with ULD, unlike the control group, showed significant ipsilateral dominance while performing a gross manual dexterity task using a prosthesis

Mechanism

  • Reduced levels of the inhibitory amino acid neurotransmitter gamma amino butyric acid (GABA) found in the motor cortex of individual with congenital ULD (Hahamy et al., 2017 and Kew et al., 1194)

  • “Unmasking” (Hahamy et al., 2017) normally silenced, less specific inputs in the ipsilateral hemisphere (van den Heiligenberg 2018).

  • Higher during early childhood (i.e., critical periods) when the brain is more plastic

  • This could explain how individuals with congenital ULD can populate the neglected brain territories with other brain representations of artificial limbs to increase overall function (van den Heiligenberg 2018).

  • This can be a compensation strategy in which the existing cortical representations of the non-affected (preferred) side are been used by the affected (non-preferred) side to operate the prosthesis (Wheaton 2017 and Ruddy and Carson 2013, and Mutha et al., 2012).

Mechanism of Action

Clinical Implications

Several investigations have reported increases in motor skills, motor learning, and motor performance in the affected, untrained upper limb after training the non-affected limb

The ipsilateral dominance found in the present investigation may provide an opportunity to effectively train the non-affected side to improve the functional performance of the affected side using prosthetic simulators.

The Team

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