What do the basal ganglia do?

doi:10.1016/S0140-6736(97)11225-9

The Lancet

Volume 351, Issue 9118, 13 June 1998, Pages 1801-1804

https://doi.org/10.1016/S0140-6736(97)11225-9 Get rights and content

Summary

We propose that the basal ganglia support a basic attentional mechanism operating to bind input to output in the executive forebrain. Such focused attention provides the automatic link between voluntary effort, sensory input, and the calling up and operation of a sequence of motor programmes or thoughts. The physiological basis for this attentional mechanism may lie in the tendency of distributed, but related, cortical activities to synchronise in the _ (30 to 50 Hz) band, as occurs in the visual cortex.¹ Coherent and synchronised elements are more effective when convergence occurs during successive stages of processing, and in this way may come together to give the one gestalt or action. We suggest that the basal ganglia have a major role in facilitating this aspect of neuronal processing in the forebrain, and that loss of this function contributes to parkinsonism and abulia.

Section snippets

Focused attention

Usually, damage to the basal ganglia leads to motor akinesia and a kind of psychic akinesia termed abulia, in which there is apathy but not dysphoria. Common to these phenomena is a disconnection of input from output, so that neither thought nor sensory information are linked to mental or physical action. We propose that a form of focused attention is necessary for the automatic binding of input to output. Only with such attention to an object or situation will voluntary effort lead to the

Physiological basis to focused attention

What is the physiological basis of this focused attention? Studies of the sensory system suggest that the brain is able to focus on and group together particular aspects of the distributed neuronal responses to a specific sensory stimulus, by making these responses coherent in frequency.1, 6 Coherent and synchronised (temporally coincident) elements are assumed to be more effective when convergence occurs during later stages of processing, so that particular channels of activity can be favoured

Clinical implications

What does focused attention mean in practice? The motor areas of the cortex (sensorimotor, lateral premotor and dorsolateral prefrontal cortices, and supplementary and cingulate motor areas) may select and group together particular aspects of the distributed neuronal responses related to an intended movement, by making these responses coherent in the _ band. We suggest that the basal ganglia facilitate this process, thereby focusing attention on what is relevant among the plethora of activities

Pathophysiological implications

The functional effects of the deranged output of the basal ganglia are likely to be the result of complex interactions between the direct and indirect pathways. We propose that reduction in the overactivity of GPi in Parkinson's disease produced by treatment with levodopa (or through high-frequency stimulation with implanted electrodes) increases thalamo-cortical activity, which releases the motor areas of the cortex from slow idling rhythms and restores the Piper rhythm. Inhibition of the

Hypothesis

Our hypothesis is that a major function of the basal ganglia is to facilitate the synchronisation of cortical activity underlying the selection and promulgation of an appropriate movement, or indeed an appropriate sequence of thoughts.

Testing the hypothesis

The hypothesis may be tested by using modern MEG techniques to demonstrate directly that the coherence at around 40 Hz between motor cortex and muscle during normal movement is lost when patients with parkinsonism are withdrawn from levodopa. Whether synchronisation in the γ range is excessive in Huntington's chorea and levodopa-induced dyskinesias (or even schitzophrenia or mania) could also be established through recordings of the Piper rhythm of muscle and the _ activity in EEG and MEG.

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Oscillatory waveform sharpness asymmetry changes in motor thalamus and motor cortex in a rat model of Parkinson's disease
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Parkinson's disease (PD) causes bursty and oscillatory activity in basal ganglia output that is thought to contribute to movement deficits through impact on motor thalamus and motor cortex (MCx). We examined the effect of dopamine loss on motor thalamus and motor cortex activity by recording neuronal and LFP activities in ventroanterior-ventrolateral (VAVL) thalamus and MCx in urethane-anesthetised control and parkinsonian rats. Dopamine lesion decreased the firing rate and increased the bursting of putative pyramidal neurons in layer V, but not layer VI, of the MCx without changing other aspects of firing pattern. In contrast, dopamine lesion did not affect VAVL firing rate, pattern or low threshold calcium spike bursts. Slow-wave (~1 Hz) oscillations in LFP recordings were analyzed with conventional power and waveform shape analyses. While dopamine lesion did not influence total power, it was consistently associated with an increase in oscillatory waveform sharpness asymmetry (i.e., sharper troughs vs. peaks) in both motor thalamus and MCx. Furthermore, we found that measures of sharpness asymmetry were positively correlated in paired motor thalamus-MCx recordings, and that correlation coefficients were larger in dopamine lesioned rats. These data support the idea that dysfunctional MCx activity in parkinsonism emerges from subsets of cell groups (e.g. layer V pyramidal neurons) and is evident in the shape but not absolute power of slow-wave oscillations. Hypoactive layer V pyramidal neuron firing in dopamine lesioned rats is unlikely to be driven by VAVL thalamus and may, therefore, reflect the loss of mesocortical dopaminergic afferents and/or changes in intrinsic excitability.
Altered Sensory Representations in Parkinsonian Cortical and Basal Ganglia Networks
2021, Neuroscience
In parkinsonian conditions, network dynamics in the cortical and basal ganglia circuits present abnormal oscillations and periods of high synchrony, affecting the functionality of multiple striatal regions including the sensorimotor striatum. However, it is still unclear how these altered dynamics impact on sensory processing, a key feature for motor control that is severely impaired in parkinsonian patients. A major confound is that pathological dynamics in sensorimotor networks may elicit unspecific motor responses that may alter sensory representations through sensory feedback, making it difficult to disentangle motor and sensory components. To address this issue, we studied sensory processing using an anesthetized model with robust sensory representations throughout cortical and basal ganglia sensory regions and limited motor confounds in control and hemiparkinsonian rats. A general screening of sensory-evoked activity in large populations of neurons recorded in the primary sensory cortex (S1), dorsolateral striatum (DLS) and substantia nigra pars reticulata (SNr) revealed increased excitability and altered sensory representations in the three regions. Further analysis revealed uncoordinated population dynamics between DLS and S1/SNr. Finally, DLS lesions in hemiparkinsonian animals partially recovered population dynamics and execution in the rotarod.
Non-invasive brain stimulation for Parkinson's disease: Clinical evidence, latest concepts and future goals: A systematic review
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Parkinson’s disease (PD) is becoming a major public-health issue in an aging population. Available approaches to treat advanced PD still have limitations; new therapies are needed. The non-invasive brain stimulation (NIBS) may offer a complementary approach to treat advanced PD by personalized stimulation. Although NIBS is not as effective as the gold-standard levodopa, recent randomized controlled trials show promising outcomes in the treatment of PD symptoms. Nevertheless, only a few NIBS-stimulation paradigms have shown to improve PD’s symptoms. Current clinical recommendations based on the level of evidence are reported in Table 1 through Table 3. Furthermore, novel technological advances hold promise and may soon enable the non-invasive stimulation of deeper brain structures for longer periods.
Destroyed non-dopaminergic pathways in the early stage of Parkinson's disease assessed by posturography
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Citation Excerpt :
The main difficulty is whether or not to increase the dose of levodopa. The quality of life is deteriorated with dyskinesia but the exaggerated bradykinesis also has a negative effect on the patients’ daily lives (Marsden, 1994; Brown and Marsden, 1998). According to our study, patients with dyskinesia have a vulnerable postural instability, which leads to falls.
The early stage of Parkinson’s disease (PD) (Hoehn-Yahr (HY) I-II stages) is characterized by a negative pull test, which clinically excludes postural instability. Previous studies with dynamic posturography detected balance disturbances even at the onset of the disease but the age dependency or prediction of dyskinesia with dynamic posturography are not known.
We hypothesized that the postural instability evoked by dynamic posturography was part of the early stage of PD. Furthermore, we studied how we can provoke dyskinesia.
Postural instability with static and dynamic posturography (passing balls with different weights around the body) was studied in 45 patients with PD in their HY I, II stages. They were compared with 35 age-matched healthy controls. Eighteen patients with dyskinesia were involved in the study. Fourteen patients were followed for two years.
The pathway and velocity of the movement assessed by static and the dynamic posturography were significantly higher in the group >65 years than that of age-matched healthy controls, while the group ≤65 years showed a significant increment only in the antero-posterior sway during dynamic posturography. The imbalance of patients with dyskinesia was significantly (p < 0.05) provoked by dynamic posturography compared to patients with PD without dyskinesia. The results were independent of age.
Postural instability is part of the early symptoms of PD. Non-dopaminergic pathways may be involved in the early stage of PD.
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We aimed to study the effect of deep brain stimulation (DBS) in the subthalamic nucleus (STN) and caudal zona incerta (cZi) on level of perceived voice tremor in patients with Parkinson disease (PD).
This is a prospective nonrandomized design with consecutive patients.
Perceived voice tremor was assessed in patients with PD having received either STN-DBS (8 patients, 5 bilateral and 3 unilateral, aged 43.1–73.6 years; median = 61.2 years) or cZi-DBS (14 bilateral patients, aged 39.0–71.9 years; median = 56.6 years) 12 months before the assessment. Sustained vowels that were produced OFF and ON stimulation (with simultaneous l-DOPA medication) were assessed perceptually in terms of voice tremor by two raters on a four-point rating scale. The assessments were repeated five times per sample and rated in a blinded and randomized procedure.
Three out of the 22 patients (13%) were concluded to have voice tremor OFF stimulation. Patients with PD with STN-DBS showed mild levels of perceived voice tremor OFF stimulation and a group level improvement. Patients with moderate/severe perceived voice tremor and cZi-DBS showed marked improvements, but there was no overall group effect. Six patients with cZi-DBS showed small increases in perceived voice tremor severity.
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View all citing articles on Scopus

View full text

HypothesisWhat do the basal ganglia do?

Summary

Section snippets

Focused attention

Physiological basis to focused attention

Clinical implications

Pathophysiological implications

Hypothesis

Testing the hypothesis

Trends Neuroci

Trends Neurosci

Prog Brain Res

Lancet

Electroencephalog Clin Neurophysiol

Neurosci Lett

Neurosci Lett

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Brain Res

Oscillatory responses in cat visual cortex exhibit inter-columnar syncrhonisation which reflects global stimulus properties

Nature

Multiple output channels in the basal ganglia

Science

The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease

Brain

Selective attention enhances the auditory 40 Hz transient response in humans

Nature

Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system

Science

Neurophysiology on man

JNeurol Neurosurg Psychiatry

Elektrophysiologie menschlicher Muskeln

The tetanic nature of the voluntary contraction in man

JPhysiol

Hypothesis
What do the basal ganglia do?