Edited by: Ahmed A. Moustafa, University of Western Sydney, Australia
Reviewed by: Calixto Machado, Institute of Neurology and Neurosurgery, Cuba; Jorge L. Morales-Quezada, Laboratory of Neuromodulation, USA
*Correspondence: Gerry Leisman, The National Institute for Brain and Rehabilitation Sciences, ORT-Braude College of Engineering, 51 Snunit, PO Box 78, Karmiel 21982, Israel e-mail:
This article was submitted to the journal Frontiers in Systems Neuroscience.
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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.
It is known that the basal ganglia interact closely with the frontal cortex (Alexander et al.,
The basal ganglia are part of a neuronal system that includes the thalamus, the cerebellum, and the frontal lobes. Like the cerebellum, the basal ganglia were previously thought to be primarily involved in motor control. However the role of the basal ganglia in motor and cognitive functions has now been well established (Alexander et al.,
The basal ganglia surround the diencephalon and are made up of five subcortical nuclei (represented in Figure
The pars compacta contains dopaminergic neurons that contain the internum. The globus pallidus internum and the pars reticulata of the putamen are the major output nuclei of the basal ganglia. The globus pallidus internum and the pars reticulata of the putamen are similar in cytology, connectivity, and function. These two nuclei can be considered to be a single structure divided by the internal capsule. Their relationship is similar to that of the caudate and the putamen. The basal ganglia are part of the extrapyramidal motor system as opposed to the pyramidal motor system that originates from the sensory-motor cerebral cortex. The pyramidal motor system is responsible for all voluntary motor activities, except for eye movement. The extrapyramidal system modifies motor control and is thought to be involved with higher-order cognitive aspects of motor control as well as in the planning and execution of complex motor strategies and the voluntary control of eye movements. There are two major pathways in the basal ganglia: the direct pathways that promote movement and the indirect pathways that inhibit movement (cf. Melillo and Leisman,
The basal ganglia receive afferent input from the entire cerebral cortex but especially from the frontal lobes. Almost all afferent connections to the basal ganglia terminate in the neo-striatum (caudate and putamen). The neo-striatum receives afferent input from two major sources outside of the basal ganglia: the cerebral cortex (cortico-striatal projections) and the intra-laminar nucleus of the thalamus. The cortico-striatal projections contain topographically organized fibers originating from the entire cerebral cortex. An important component of that input comes from the centro-median nucleus and terminates in the putamen. Because the motor cortex of the frontal lobes projects to the centro-median nucleus, this may be an additional pathway by which the motor cortex can influence the basal ganglia. The putamen appears to be primarily concerned with motor control, whereas the caudate appears to be involved in the control of eye movements and certain cognitive functions. The ventral striatum is related to limbic function and therefore may affect autonomic and emotional functions.
The major output of the basal ganglia arises from the internal segment of the globus pallidus and the pars reticulata of the putamen. The nuclei project in turn to three nuclei in the thalamus: the ventral lateral nuclei, the ventral anterior nuclei, and the mesio-dorsal nuclei. Internal segments of the globus pallidus project to the centro-median nucleus of the thalamus. Striatal neurons may be involved with gating incoming sensory input to higher motor areas such as the intra-laminar thalamic nuclei and premotor cortex that arise from several modalities to coordinate behavioral responses. These different modalities may contribute to the perception of sensory input (Middleton and Strick,
Experiments where herpes simplex virus-1 was administered into the dorsolateral prefrontal cortex of monkeys to determine its axonal spread or connection labeled the ipsilateral neurons in the internal segments of the globus pallidus and the contralateral dentate nucleus of the cerebellum (Chudler and Dong,
The putamen is also thought to connect to the superior colliculus through non-dopaminergic axons, which forms an essential link in voluntary eye movement. It is thought that the normal basal ganglia function results from a balance of the direct and indirect striatal output pathways and the different involvement of these pathways account for hyperkinesia or hypokinesia observed in disorders of the basal ganglia (Middleton and Strick,
Five fronto-subcortical circuits unite regions of the frontal lobe (the supplementary motor area; frontal eye fields; and dorsolateral, prefrontal, orbitofrontal, and anterior cingulate cortices) with the striatum, the globus pallidus, and the thalamus in functional systems that mediate volitional motor activity, saccadic eye movements, executive functions, social behavior, and motivation (Litvan et al.,
In general then, there exist a number of cortical loops through the basal ganglia that involve prefrontal association cortex and limbic cortex. Through these loops, the basal ganglia are thought to play a role in cognitive function that is similar to their role in motor control. That is, the basal ganglia are involved in selecting and enabling various cognitive, executive, or emotional programs that are stored in these other cortical areas. Moreover, the basal ganglia appear to be involved in certain types of learning. For example, in rodents the striatum is necessary for the animal to learn certain stimulus-response tasks (e.g., make a right turn if stimulus A is present and make a left turn if stimulus B is present). Recordings from rat striatal neurons show that early in training, striatal neurons fire at many locations while a rat learns in a T-shaped maze. This suggests that initially the striatum is involved throughout the execution of the task. As the animal learns the task and becomes exceedingly good at its performance, the striatal neurons change their activity patterns, firing only at the beginning of the trial and at the end. It appears that the learned programs to solve this task are now stored elsewhere; the firing of the striatal neurons at the beginning of the maze presumably reflects the enabling of the appropriate motor/cognitive plan in the cortex, and the firing at the end of the maze is presumably involved in evaluating the reward outcome of the trial.
Some circuits in the basal ganglia are involved in non-motor aspects of behavior. These circuits originate in the prefrontal and limbic regions of the cortex and engage specific areas of the striatum, pallidum, and substantia nigra. The dorsolateral prefrontal circuit originates in Brodmann's areas 9 and 10 and projects to the head of the caudate nucleus, which then projects directly and indirectly to the dorsomedial portion of the internal pallidal segment and the rostral substantia nigra pars reticulata. Projections from these regions terminate in the ventral anterior and medial dorsal thalamic nuclei, which in turn project back upon the dorsolateral prefrontal area. The dorsolateral prefrontal circuit has been implicated broadly in so-called “executive functions.” These include cognitive tasks such as organizing behavioral responses and using verbal skills in problem solving. Damage to the dorsolateral prefrontal cortex or subcortical portions of the circuit are associated with a variety of behavioral abnormalities related to these cognitive functions.
The lateral orbitofrontal circuit arises in the lateral prefrontal cortex and projects to the ventromedial caudate nucleus. The pathway from the caudate nucleus follows that of the dorsolateral circuit (through the internal pallidal segment and substantia nigra pars reticulata and thence to the thalamus) and returns to the orbitofrontal cortex. The lateral orbitofrontal cortex appears to play a major role in mediating empathetic and socially appropriate responses. Damage to this area is associated with irritability, emotional lability, failure to respond to social cues, and lack of empathy. A neuro-psychiatric disorder thought to be associated with disturbances in the lateral orbitofrontal cortex and circuit is obsessive-compulsive disorder.
The anterior cingulate circuit arises in the anterior cingulate gyrus and projects to the ventral striatum. The ventral striatum also receives “limbic” input from the hippocampus, amygdala, and entorhinal cortices. The projections of the ventral striatum are directed to the ventral and rostromedial pallidum and the rostrodorsal substantia nigra pars reticulata. From there the pathway continues to neurons in the paramedian portion of the medial dorsal nucleus of the thalamus, which in turn project back upon the anterior cingulate cortex. The anterior cingulate circuit appears to play an important role in motivated behavior, and it may convey reinforcing stimuli to diffuse areas of the basal ganglia and cortex via inputs through the ventral tegmental areas and the substantia nigra pars compacta (SNpc). These inputs may play a major role in procedural learning. Damage to the anterior cingulate region bilaterally can cause akinetic mutism, a condition characterized by profound impairment of movement initiation.
In general, the disorders associated with dysfunction of the prefrontal cortex and cortico-basal ganglia-thalamo-cortical circuits involve action rather than of perception or sensation. These disturbances are associated both with both intensified action (impulsivity) and flattened action (apathy). Obsessive-compulsive behavior can be viewed as a form of hyperactivity. The disturbances of mood associated with circuit dysfunction are believed to span the extremes of mania and depression. Both dopamine and serotonin, two biogenic amines that modulate neuronal activity within the circuits, are important to depression.
These observations suggest that the neural mechanisms underlying complex behavioral disorders might be analogous to the dysfunctions of motor circuits. Thus, schizophrenia might be viewed as a “Parkinson disease of thought.” By this analogy, schizophrenic symptoms would arise from disordered modulation of prefrontal circuits. Other cognitive and emotional symptoms may similarly be equivalents of motor disturbances such as tremor, dyskinesia, and rigidity.
In humans, the basal ganglia appear to be necessary for certain forms of implicit memory tasks. Like motor habit learning, many types of cognitive learning require repeated trials and are often unconscious. An example is probabilistic classification. In this type of task, people have to learn to classify objects based on the probability of belonging to a class, rather than on any explicit rule. In one experiment, subjects were shown a deck of cards with different symbols. Each symbol was associated with a certain probability of predicting rain or sunshine, and the subjects had to say on each trial whether the symbol was a predictor of rain or sunshine. Because the same symbol sometimes predicted sunshine and other times predicted rain, the subjects could not devise a simple rule, and they made many errors at first. Over time, however, they began to get better at classifying the symbols appropriately, although they still often claimed to be guessing. Patients with basal ganglia disorders were impaired at this task, suggesting that the processing of the cognitive loops of the basal ganglia are somehow involved in our ability to subconsciously learn the probabilities of predicted outcomes associated with particular stimuli.
Some circuits in the basal ganglia are involved in non-motor aspects of behavior. These circuits originate in the prefrontal and limbic regions of the cortex and engage specific areas of the striatum, pallidum, and substantia nigra. The dorsolateral prefrontal circuit originates in Brodmann's areas 9 and 10 and projects to the head of the caudate nucleus, which then projects directly and indirectly to the dorsomedial portion of the internal pallidal segment and the rostral substantia nigra pars reticulata. Projections from these regions terminate in the ventral anterior and medial dorsal thalamic nuclei, which in turn project back upon the dorsolateral prefrontal area. The dorsolateral prefrontal circuit has been implicated broadly in so-called “executive functions.” These include cognitive tasks such as organizing behavioral responses and using verbal skills in problem solving. Damage to the dorsolateral prefrontal cortex or subcortical portions of the circuit are associated with a variety of behavioral abnormalities related to these cognitive functions.
The lateral orbitofrontal circuit arises in the lateral prefrontal cortex and projects to the ventromedial caudate nucleus. The pathway from the caudate nucleus follows that of the dorsolateral circuit (through the internal pallidal segment and substantia nigra pars reticulata and thence to the thalamus) and returns to the orbitofrontal cortex. The lateral orbitofrontal cortex appears to play a major role in mediating empathetic and socially appropriate responses. Damage to this area is associated with irritability, emotional lability, failure to respond to social cues, and lack of empathy. A neuro-psychiatric disorder thought to be associated with disturbances in the lateral orbitofrontal cortex and circuit is obsessive-compulsive disorder.
The anterior cingulate circuit arises in the anterior cingulate gyrus and projects to the ventral striatum. The ventral striatum also receives “limbic” input from the hippocampus, amygdala, and entorhinal cortices. The projections of the ventral striatum are directed to the ventral and rostromedial pallidum and the rostrodorsal substantia nigra pars reticulata. From there the pathway continues to neurons in the paramedian portion of the medial dorsal nucleus of the thalamus, which in turn project back upon the anterior cingulate cortex. The anterior cingulate circuit appears to play an important role in motivated behavior, and it may convey reinforcing stimuli to diffuse areas of the basal ganglia and cortex via inputs through the ventral tegmental areas and the SNpc. These inputs may play a major role in procedural learning. Damage to the anterior cingulate region bilaterally can cause akinetic mutism, a condition characterized by profound impairment of movement initiation.
In general, the disorders associated with dysfunction of the prefrontal cortex and cortico-basal ganglia-thalamo-cortical circuits involve action rather than perception or sensation. These disturbances are associated both with both intensified action (impulsivity) and flattened action (apathy). Obsessive-compulsive behavior can be viewed as a form of hyperactivity. The disturbances of mood associated with circuit dysfunction are believed to span the extremes of mania and depression. Both dopamine and serotonin, two biogenic amines that modulate neuronal activity within the circuits, are important to depression (Leisman and Melillo,
These observations suggest that the neural mechanisms underlying complex behavioral disorders might be analogous to the dysfunctions of motor circuits. Thus, schizophrenia might be viewed as a “Parkinson disease of thought.” By this analogy, schizophrenic symptoms would arise from disordered modulation of prefrontal circuits. Other cognitive and emotional symptoms may similarly be equivalents of motor disturbances such as tremor, dyskinesia, and rigidity.
In humans, the basal ganglia appear to be necessary for certain forms of implicit memory tasks. Like motor habit learning. Many types of cognitive learning require repeated trials and are often unconscious. An example is probabilistic classification (Figure
It has been known for a while that individuals who are markedly late in achieving developmental milestones are at high risk for subsequent cognitive impairment (von Wendt et al.,
The developing infant is concerned with navigating to items of interest and exploring the environment, ultimately to develop a sense of self, independent of the environment to which he or she is circumnavigating. The central idea of the mechanism being advocated concerns the influence on a proceeding (or currently planned) muscular act. That influence stems from motivation-triggered anticipation of the act's outcome, and it is conjectured to prevail only if “consciousness” is present.
Because motivation relates to the self, while an act's consequences can include environmental components, consciousness is seen as lying at the operational interface between body movement and the body's surroundings. Anticipation is mediated by specific anatomical features, the independent functioning of which, underlies thought simulation of the body's (sometimes passive) transactions with its milieu. Only through those anatomical attributes can an individual possess consciousness.
When a child attempts its first step, prior attainment of the balanced upright position will have involved failed attempts, with attendant pain. What leads to discomfort will have been stored as memory of possible sensory feedback resulting from certain self-paced movements. Likewise, the fact that specific muscular movements can achieve forward motion will already be part of a repertoire accessible unconsciously. Ultimately, the child hits upon the correct combination and timing of elemental movements and the first successful step is taken. That consolidation into a more complex motor pattern is temporarily deposited in explicit memory (Squire,
The system conjures up a simulated probable outcome of the intended motor pattern, and vetoes it if the prognosis is adverse. The simulated outcome lies below the threshold for actual movement, and the mimicking requires two-way interaction between the nervous system and the spindles (Matthews,
The bottleneck in sensory processing (Broadbent,
We can think without acting, act without thinking, act while thinking about that act, and act while thinking about something else. Our acts can be composite, several muscular patterns being activated concurrently, though we appear not to be able to simultaneously maintain two streams of thought. When we think about one thing while doing something else, it is always our thoughts, which are the focus of attention. This suggests that there are least two thresholds, the higher associated with overt movement and the lower with thought. Assuming that the signals underlying competing potential thoughts must race each other to a threshold (Carpenter et al.,
The competition (Posner and Rothbart,
The focus of competition for attention appears to be the PMA/SMA, because it receives from all the thalamic nuclei handling BG/Cb output. More remote regions of the system, which feed signals to those BG/Cb components, influence attention. The inferior olive seems to play a complementary role for the Cb, sending signals through the climbing fibers when something unexpected occurs (De Zeeuw et al.,
Thoughts, according to this scheme, are merely simulated interactions with the environment, and their ultimate function is the addition of new implicit memories, new standard routes from sensory input to permitted motor output or new optimized complex reflexes. For a given set of synaptic couplings between PMA/SMA and M1, a specific pattern of output signals from the former will produce a specific sequence of muscular movements. Efference copies of those output signals, dispatched through axon collaterals, will carry the full information sent to the muscles, via M1, but they will not directly produce movement because their target neurons are not immediately concerned with motor output. Those efference-copy signals may be above the threshold for thought, however, and the latter will thus be subtly tied to a pattern of motor output. The duality of routes, and the fact that these overlap in the PMA/SMA region, could well underlie the interplay between explicit and implicit in brain function.
A major problem confronting those who would explain consciousness is its apparently multifarious nature and the attendant difficulty in an effective operational definition. We attach great significance to the provision of context-specific reflexes, as occurs when one is learning to walk.
At the largest scale, one can see a number of parallel loops from the frontal cortex to the striatum to the globus pallidus internal segment (GPi) or substantia nigra pars reticulata (SNr) and then on to the thalamus, finally projecting back up in the frontal cortex (Alexander et al.,
Here we will discuss the implications of a few important anatomical properties of the basal-ganglia-frontal-cortex system. A strong constraint on understanding basal ganglia function comes from the fact that the GPi and SNr have a relatively small number of neurons. There are approximately 111 million neurons in the human striatum (Fox and Rafols,
Another constraint to consider concerns the number of different sub-regions of the frontal cortex for which the basal ganglia can plausibly provide separate gating control. Crude estimates suggest that gating occurs at a relatively fine-grained level. Fine-grained gating is important for mitigating conflicts where two representations require separate gating control and yet fall within one gating region. The number of neurons in the GPi/SNr provides an upper limit estimate, which is roughly 320,000 in the human. This suggests that the gating signal operates on a region of frontal neurons, instead of individually controlling specific neurons.
An interesting possible candidate for the regions of the frontal cortex that are independently controlled by the basal ganglia are distinctive anatomical structures consisting of interconnected groups of neurons, called stripes (Pucak et al.,
Anatomical constraints are consistent with the selective gating hypothesis by suggesting that the basal ganglia interacts with a large number of distinct regions of the frontal cortex. We hypothesize that these distinct stripe structures constitute separately gated col- lections of frontal neurons, extending the parallel loops concept of Alexander et al. (
The nature of primitive reflex development on both motor and cognitive function has been more extensively reviewed elsewhere (Melillo,
In another study (Burns et al.,
In yet another study, (Dutia et al.,
Romeo et al. (
Teitelbaum et al. (
Although there exist numerous definitions of intelligence beyond one's ability to perform on intelligence tests, in the context of our present discussion, it is possible to define intelligence operationally as, “
When a new motor pattern is being acquired, both the means and the ends will be coded in currently active patterns of neuronal signals. And there must be interactions between these patterns because the goal will influence the route through muscular hyper- space by which it is to be achieved. The PFC probably dictates patterns of elementary muscular sequences, but it must be borne in mind that the sophistication of the latter will depend upon what the individual has already learned. A ballet dancer would regard as an elementary motor pattern a muscular sequence, which the novice would find quite difficult. The most spectacular feature to evolve thus far has been that seen in the mammals, and it permitted acquisition, during a creature's own lifetime, of novel context-specific reflexes, especially those relying on sequences of muscular movements. This mechanism makes heavy demands on the neural circuitry, because it requires an attentional mechanism. And because attention must, perforce, be an active process, there has to be feedback from the muscles, carrying information about their current state, including their current rate of change of state. Without such information, anticipation would be impossible, and without anticipation there could be no meaningful adjudication and decision as to the most appropriate way of continuing an on-going movement. Without such a mechanism, novel context-specific reflexes could not be acquired.
The fascinating thing is that access to such on-line information mediates consciousness, the gist of which is the ability to know that one knows. The ability to know that one knows is referred to by psychologists as first-order embedding. Higher embedding, such as that exemplified by knowing that one knows that one knows, merely depends upon the ability to hold things in separate patches of neuronal activity in working memory. This manifests itself in a creature's intelligence, which also dictates its ability to consolidate existing schemata into a new schema. When we know that we know, the muscular apparatus is not only monitoring its own state, it is monitoring the monitoring.
In short, one can think of the overall influence of the basal ganglia on the frontal cortex as “releasing the brakes” for motor actions and other functions. The basal ganglia are important for initiating motor movements, but not for determining the detailed properties of those movements.
We have elsewhere described how abnormal motor development can accurately be used as a marker to predict autism and other developmental disorders in later development (Leisman,
Postural sway during quiet stance is often assumed to be a resultant sum of internal noises generated in the postural control system carrying little useful information (Ishida and Imai,
Although “time to maintain a given posture” is a useful clinical measure, “body sway” is used as a measure to characterize the performance of upright posture. Body sway is a kinematic term and can be derived from the sum of forces and moments acting on the human body. Many studies have shown that when various sensory systems are systematically manipulated, body sway is affected (Masani et al.,
The most simplified biomechanical model assumes the human as one rigid body, where the COM is located at the waist, a pivot axis at the ankle, and a COP where the GRF vector acts. The assumptions used in the presented model are those of the inverted pendulum model of human standing balance (Winter and Eng,
From Euler's equation:
A major problem for human standing posture is the high center of gravity (COG) maintained over a relatively small base of support.
In attempting to understand motor mechanisms involved in the development of balance, research on postural control has focused mainly on two types of study: (a) balance with respect to external conditions, (b) postural adjustments to anticipated internal disturbances of balance. Unexpected external disturbances reveal centrally programmed patterns of postural responses. Afferent feedback also influences posture when the initial setting is disturbed. The second type of disturbance reveals feed-forward postural adjustments (for review, Dietz,
Studies of the postural responses to unexpected small and slow external disturbances in the antero-posterior direction found that most people reposition the COG by swaying as a flexible inverted pendulum primarily about the ankles with little hip or knee motion. This stereotyped pattern of muscle activation is called “ankle strategy.” When responding to larger, faster displacement of support, the primary action of most people occurs at the hip resulting in active trunk rotation or the so-called “hip strategy” (Nashner and McCollum,
Locomotion is fundamental for an optimal child development. The ability to smoothly and adequately navigate through the environment enables the child to interact with the environment. Children with developmental disabilities including autism spectrum disorders and attention deficit/hyperactivity disorder (ADHD) demonstrate locomotor difficulties. ADHD and autistic spectrum individuals have reported significant motor difficulties, both fine and gross (Melillo and Leisman,
According to Patla et al. (
Similar neuromuscular problems, indicating difficulties with the selective muscle control necessary for rhythmic coordination, were found in a unilateral tapping task by Lundy-Ekman et al. (
So far, descriptions of the gait pattern of children with DCD are limited to some qualitative observations. Larkin and Hoare (
Up to 50% of children and adolescents with ADHD exhibit motor abnormalities including altered balance (Buderatha et al.,
In a Dutch study (Hadders-Algra and Towen,
In Asperger's syndrome, it has been noted that individual's have significant degrees of motor incoordination. In fact, in Wing's original paper, she noted that of the 34 cases that she had diagnosed based on Asperger's description, “90% were poor at games involving motor skill, and sometimes the executive problems affect their ability to write or draw.” Although, gross motor skills are most frequently affected, fine motor and specifically graphomotor skills were sometimes considered significant in Asperger's syndrome” (Wing,
Gillberg and Gillberg (
It has been reported (Gillberg and Kadesjö,
Manjiviona and Prior (
Kohen-Raz et al. (
Makris et al. (
Researchers at Stanford University have observed that in children with ADHD, also known as childhood hyperkinetic disorder (Wing and Attwood,
This may be a similar finding as the PET scans on patients with hyperactivity disorder, where normal appearing frontal metabolism existed with decreased caudate and putamen metabolism (Gillberg and Gillberg,
Etiological theories suggest a deficit in cortico-striatal circuits, particularly those components modulated by dopamine and therefore discussed in comparison with the other basal ganglia related disorders in the paper. Teicher et al. (
Converging evidence implies the involvement of dopaminergic fronto-striatal circuitry in ADHD. Anatomical imaging studies using MRI have demonstrated subtle reductions in volume in regions of the basal ganglia and prefrontal cortex (Castellanos et al.,
Volumetric abnormalities have also been associated with the basal ganglia and in turn with ADHD. Qiu et al. (
Aaron et al. (
Balance deficits, motor planning, motor coordination and perceptual-motor problems associated with other developmental disorders are, as we have noted, present with individuals with ADHD (Kaplan et al.,
The contribution of sensory organs to posture has been the object of much inquiry and for good reason. A malfunction in any of the three primary sensory subsystems (visual, vestibular, or somatosensory) can compromise integrative function and as a result limit adaptability of posture. A lack of optimal postural control limits the development of sensory strategies, anticipatory mechanisms, internal representations, neuromuscular synergies, and adaptive mechanisms (Shumway-Cook and Woolacott,
Inadequate input and the inability to integrate and prioritize information from different sources result in instability, poor motor planning, poor coordination, and perceptual motor problems. Although posture dysfunction among children with ADHD may not be easily identified, research indicates that balance is compromised with this population (Zang et al.,
Posture and balance are accomplished through several mechanisms acting together to maintain orientation and stability (Shumway-Cook and Woolacott,
Self-organizing properties of motor behavior evident in other biological and natural systems are evident in the developing human as well (Kamm et al.,
In postural terms, early forms of coordinative units that allow infants to interact with the environment necessitate reflexes. Through development, more complex forms of control emerge such as anticipatory postural responses (e.g., feed-forward mechanisms, Horak and Nashner,
Dysfunction may arise because a subcomponent of the system is not functioning to its capacity, thus acting as a weak link. Children with ADHD interact with their environment but not in a consistent fashion as the typical population, perhaps due to a less than adequate sensory apparatus as suggested (Zang et al.,
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 including those associated with frontal lobes. Many neocortical and subcortical regions support the cortical-striatal-cortical circuits that confer various aspects of language ability, for example. However, many of these structures also form part of the neural circuits regulating other aspects of behavior. For example, the basal ganglia, which regulate motor control, are also crucial elements in the circuits that confer human linguistic ability and reasoning. The cerebellum, traditionally associated with motor control, is active in motor learning. The basal ganglia are also key elements in reward-based learning. Data from studies individuals with Tourette's syndrome, Obsessive-Compulsive Disorder as well as with Broca's aphasia, Parkinson's disease, hypoxia, focal brain damage, and from comparative studies of the brains and behavior of other species, demonstrate that the basal ganglia sequence the discrete elements that constitute a complete motor act, syntactic process, or thought process. Imaging studies of intact human subjects and electrophysiologic and tracer studies of the brains and behavior of other species confirm these findings. Dobzansky had stated, “Nothing in biology makes sense except in the light of evolution” (cited in Mayr,
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This work has been supported, in part, by the Government of Israel,