Cognitive-motor interactions of the basal ganglia in development

Abstract

Neural circuits linking activity in anatomically segregated populations of neurons in subcortical structures and the neocortex throughout the human brain regulate complex behaviors such as walking, talking, language comprehension, and other cognitive functions associated with frontal lobes. The basal ganglia, which regulate motor control, are also crucial elements in the circuits that confer human reasoning and adaptive function. The basal ganglia are key elements in the control of reward-based learning, sequencing, discrete elements that constitute a complete motor act, and cognitive function. Imaging studies of intact human subjects and electrophysiologic and tracer studies of the brains and behavior of other species confirm these findings. We know that the relation between the basal ganglia and the cerebral cortical region allows for connections organized into discrete circuits. Rather than serving as a means for widespread cortical areas to gain access to the motor system, these loops reciprocally interconnect a large and diverse set of cerebral cortical areas with the basal ganglia. Neuronal activity within the basal ganglia associated with motor areas of the cerebral cortex is highly correlated with parameters of movement. Neuronal activity within the basal ganglia and cerebellar loops associated with the prefrontal cortex is related to the aspects of cognitive function. Thus, individual loops appear to be involved in distinct behavioral functions. Damage to the basal ganglia of circuits with motor areas of the cortex leads to motor symptoms, whereas damage to the subcortical components of circuits with non-motor areas of the cortex causes higher-order deficits. In this report, we review some of the anatomic, physiologic, and behavioral findings that have contributed to a reappraisal of function concerning the basal ganglia and cerebellar loops with the cerebral cortex and apply it in clinical applications to attention deficit/hyperactivity disorder (ADHD) with biomechanics and a discussion of retention of primitive reflexes being highly associated with the condition.

Keywords: ADHD; autism; basal ganglia; cognition; frontal lobe; posture.

Figure 1

The basal ganglia that clinically includes sub-thalamic nucleus and substantia nigra whose component structures are highly interconnected. The striatum is associated with input signal and output associated with the globus pallidus and substantia nigra.

Figure 2

Basal ganglia frontal lobe connectivities for motor cognitive interaction. All regions of the cerebral cortex project to the basal ganglia, but the output of the basal ganglia are directed toward the frontal lobe, particularly the premotor and supplementary motor cortex with specific connectivities of the basal ganglia for (A) attention, working memory, and executive function (B) conditioned fear memory and (C) cerebellar and basal ganglia modulation of cognition.

Figure 3

The basal ganglia projections and connections to other CNS regions (excitatory and inhibitory projections are shown by arrows and stars respectively). Decisions are made by several mechanisms organized hierarchically. CM, centromedian thalamus; D1, D1 receptor dominant medium spiny neurons; D2, D2 receptor dominant medium spiny neurons; GPe, external globus pallidus; GPi, internal globus pallidus; PPN/MLR, pedunculopontine nucleus; STN, subthalamic nucleus; STR, striatum; VA, ventral anterior thalamus; VL, ventral lateral thalamus (From Kamali Sarvestani et al., 2011).

Figure 4

Summary of biomechanical principles. Body center-of-mass (COM)—is the location where all of the mass of the system could be considered to be located. For a solid body it is often possible to replace the entire mass of the body with a point mass equal to that of the body's mass. This point mass is located at the center of mass. COG—the resultant force of all of small attractive forces of the mass particles of which the body is composed is the body's weight, and the location at which the resultant force is assumed to act. Ground reaction force vector (GRF)—the resultant of a pressure distribution under the foot or feet. Center- of -pressure (COP)—the location point of the ground reaction force vector (GRF). Body center-of-mass (COM) is regulated through movement of the COP under the feet. In such a model the difference between body COM and COP will be proportional to the acceleration of body COM. Base of support (BoS), is defined as the possible range of the COP, which is loosely equal to the area below and between the feet (in two-feet standing) (Winter et al., 1988).

Figure 5

Stick-figures of the body configuration at initial FS (left) and TO (right). Gray lines represent the TD-children without DCD, black lines represent the children with DCD. Feet with broken lines are the contralateral feet. Arrows indicate significant differences of the joint angles (p < 0.05) (from Deconinck, 2005).

Figure 6

Index of Walking Performance of the 10 children with and the 10 children without DCD. Values of the separate strides are indicated with ◦, means per child are indicated with +. The horizontal broken line indicates the cut-off value (2.69) according to Woodruff et al. (2002).

Figure 7

(A) The interactive race model between Go and Stop processes. The parameters were estimated by fitting the model to thousands of behavioral trials from a monkey neurophysiology study. (B) Schematic of fronto-basal-ganglia circuitry for Going and Stopping. The Go process is generated by premotor cortex, which excites striatum and inhibits globus pallidus, removing inhibition from thalamus and exciting motor cortex (see text for details). The stopping process could be generated by IFC leading to activation of the subthalamic nucleus, increasing broad excitation of pallidum and inhibiting thalamocortical output, reducing activation in motor cortex. (C) Diffusion-weighted imaging reveals putative white matter tracts in the right hemisphere between the dorsomedial preSMA, the ventrolateral PFC or IFC, and the putative region of the STN. (D) Regions of the rat brain implicated in behavioral stopping. Stopping is significantly impaired following excitotoxic lesions within the regions highlighted in red, whereas lesions within the gray-colored regions have no effect on stopping. OF, Orbitofrontal cortex; IL, infralimbic cortex; PL, prelimbic cortex; DM Str, dorsomedial striatum; NAC, nucleus accumbens (core); DH, dorsal hippocampus; VH, ventral hippocampus; GPi, globus pallidus pars interna (from Aaron and Poldrack, 2006).