Trends in Neurosciences
ReviewFunctional architecture of basal ganglia circuits: neural substrates of parallel processing
Abstract
Concepts of basal ganglia organization have changed markedly over the past decade, due to significant advances in our understanding of the anatomy, physiology and pharmacology of these structures. Independent evidence from each of these fields has reinforced a growing perception that the functional architecture of the basal ganglia is essentially parallel in nature, regardless of the perspective from which these structures are viewed. This represents a significant departure from earlier concepts of basal ganglia organization, which generally emphasized the serial aspects of their connectivity. Current evidence suggests that the basal ganglia are organized into several structurally and functionally distinct ‘circuits’ that link cortex, basal ganglia and thalamus, with each circuit focused on a different portion of the frontal lobe. In this review, Garrett Alexander and Michael Crutcher, using the basal ganglia ‘motor’ circuit as the principal example, discuss recent evidence indicating that a parallel functional architecture may also be characteristic of the organization within each individual circuit.
References (67)
- C. Asanuma et al.
Brain Res. Rev.
(1983) - H.J. Spencer
Brain Res.
(1976) - J.B. Penney et al.
Brain Res.
(1981) - G. Chevalier et al.
Brain Res.
(1985) - J.M. Deniau et al.
Brain Res.
(1985) - R.L. Albin et al.
Trends Neurosci.
(1989) - H. Nakanishi et al.
Brain Res.
(1987) - Y. Smith et al.
Brain Res.
(1988) - H. Kunzle
Brain Res.
(1975) - T.N. Johnson et al.
Exp. Neurol.
(1971)
Brain Res.
Exp. Neurol.
Brain Res.
Brain Res.
Trends Neurosci.
J. Comp. Neurol.
Annu. Rev. Neurosci.
Nature
Neuroscience
J. Neurosci.
J. Neurophysiol.
Exp. Brain Res.
Exp. Brain Res.
Biol. Psychiatry
J. Neurochem.
J. Comp. Neurol.
Exp. Brain Res.
Cited by (3361)
This paper reviews Luria's model of the three functional units of the brain. To meet this objective, several issues were reviewed: the theory of functional systems and the contributions of phylogenesis and embryogenesis to the brain's functional organization. This review revealed several facts. In the first place, the relationship/integration of basic homeostatic needs with complex forms of behavior. Secondly, the multi-scale hierarchical and distributed organization of the brain and interactions between cells and systems. Thirdly, the phylogenetic role of exaptation, especially in basal ganglia and cerebellum expansion. Finally, the tripartite embryogenetic organization of the brain: rhinic, limbic/paralimbic, and supralimbic zones. Obviously, these principles of brain organization are in contradiction with attempts to establish separate functional brain units.
The proposed new model is made up of two large integrated complexes: a primordial-limbic complex (Luria's Unit I) and a telencephalic-cortical complex (Luria's Units II and III). As a result, five functional units were delineated: Unit I. Primordial or preferential (brainstem), for life-support, behavioral modulation, and waking regulation; Unit II. Limbic and paralimbic systems, for emotions and hedonic evaluation (danger and relevance detection and contribution to reward/motivational processing) and the creation of cognitive maps (contextual memory, navigation, and generativity [imagination]); Unit III. Telencephalic-cortical, for sensorimotor and cognitive processing (gnosis, praxis, language, calculation, etc.), semantic and episodic (contextual) memory processing, and multimodal conscious agency; Unit IV. Basal ganglia systems, for behavior selection and reinforcement (reward-oriented behavior); Unit V. Cerebellar systems, for the prediction/anticipation (orthometric supervision) of the outcome of an action.
The proposed brain units are nothing more than abstractions within the brain's simultaneous and distributed physiological processes. As function transcends anatomy, the model necessarily involves transition and overlap between structures. Beyond the classic approaches, this review includes information on recent systemic perspectives on functional brain organization. The limitations of this review are discussed.
The mediodorsal thalamus in executive control
2024, NeuronExecutive control, the ability to organize thoughts and action plans in real time, is a defining feature of higher cognition. Classical theories have emphasized cortical contributions to this process, but recent studies have reinvigorated interest in the role of the thalamus. Although it is well established that local thalamic damage diminishes cognitive capacity, such observations have been difficult to inform functional models. Recent progress in experimental techniques is beginning to enrich our understanding of the anatomical, physiological, and computational substrates underlying thalamic engagement in executive control. In this review, we discuss this progress and particularly focus on the mediodorsal thalamus, which regulates the activity within and across frontal cortical areas. We end with a synthesis that highlights frontal thalamocortical interactions in cognitive computations and discusses its functional implications in normal and pathological conditions.
Diffusion tensor imaging in pediatric patients with dystonia
2024, NeuroImageBackground: Childhood-onset dystonia is often progressive and severely impairs a child´s life. The pathophysiology is very heterogeneous and treatment responses vary in patients with dystonia. Factors influencing treatment effects remain to be elucidated. We hypothesize that differences in brain connectivity and fiber coherence contribute to the heterogeneity in treatment response among pediatric patients with inherited and acquired dystonia.
Methods: Twenty patients with childhood-onset dystonia were retrospectively recruited including twelve patients with inherited or idiopathic, and eight patients with acquired dystonia (mean age 10 years; 8 female/12 male). Fiber density between the internal part of the globus pallidus and selective target regions, as well as the diffusion measures of fractional anisotropy (FA) and mean diffusivity (MD) were analyzed and compared between different etiologies.
Results: Patients with acquired dystonia presented higher fiber density to the premotor cortex and putamen and lower FA values in the thalamus compared to patients with inherited/idiopathic dystonia. MD in the premotor cortex was higher in patients with acquired dystonia, while it was lower in the thalamus.
Conclusion: Diffusion MRI reveals microstructural and network alterations in patients with dystonia of different etiologies.
Distinct neural adaptations to time demand in the striatum and the hippocampus
2024, Current BiologyHow do neural codes adjust to track time across a range of resolutions, from milliseconds to multi-seconds, as a function of the temporal frequency at which events occur? To address this question, we studied time-modulated cells in the striatum and the hippocampus, while macaques categorized three nested intervals within the sub-second or the supra-second range (up to 1, 2, 4, or 8 s), thereby modifying the temporal resolution needed to solve the task. Time-modulated cells carried more information for intervals with explicit timing demand, than for any other interval. The striatum, particularly the caudate, supported the most accurate temporal prediction throughout all time ranges. Strikingly, its temporal readout adjusted non-linearly to the time range, suggesting that the striatal resolution shifted from a precise millisecond to a coarse multi-second range as a function of demand. This is in line with monkey’s behavioral latencies, which indicated that they tracked time until 2 s but employed a coarse categorization strategy for durations beyond. By contrast, the hippocampus discriminated only the beginning from the end of intervals, regardless of the range. We propose that the hippocampus may provide an overall poor signal marking an event’s beginning, whereas the striatum optimizes neural resources to process time throughout an interval adapting to the ongoing timing necessity.
Neural population dynamics relevant to behavior vary over multiple spatial and temporal scales across three-dimensional volumes. Current optical approaches lack the spatial coverage and resolution necessary to measure and manipulate naturally occurring patterns of large-scale, distributed dynamics within and across deep brain regions such as the striatum. We designed a new micro-fiber array approach capable of chronically measuring and optogenetically manipulating local dynamics across over 100 targeted locations simultaneously in head-fixed and freely moving mice, enabling the investigation of cell-type- and neurotransmitter-specific signals over arbitrary 3D volumes at a spatial resolution and coverage previously inaccessible. We applied this method to resolve rapid dopamine release dynamics across the striatum, revealing distinct, modality-specific spatiotemporal patterns in response to salient sensory stimuli extending over millimeters of tissue. Targeted optogenetics enabled flexible control of neural signaling on multiple spatial scales, better matching endogenous signaling patterns, and the spatial localization of behavioral function across large circuits.
Decision-making ability limitations and brain neural activity changes in healthcare workers after mild COVID-19
2024, Neuroscience ResearchStudies have demonstrated that the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) extensively affects brain function. Although cognitive dysfunction is considered a common manifestation in COVID-19 patients during the recovery period, the potential changes in decision-making ability, are not yet clear. Decision-making functions are essential to the work of healthcare workers. However, there is a lack of a multidimensional assessment of its functioning in COVID-19 cases. Here, we used tests combined with the resting-state functional magnetic resonance imaging (rs-fMRI) stabilization feature amplitude of low-frequency fluctuations (ALFF) to explore decision-making behavior and brain neural activity changes in healthcare workers after mild COVID-19. Participants were divided into the SARS-CoV-2 infected group (SI, n = 41) and healthy controls (HC, n = 42). All participants underwent a series of neuropsychological tests. They performed the Iowa Gambling Task (IGT) and the Game of Dice Task (GDT), followed by fMRI (n = 20) to assess their decision-making ability under ambiguous and risky conditions and changes in brain neural activity. The SI group performed worse in verbal memory than the HC group. Furthermore, the SI group performed worse in the IGT, whereas no significant difference was observed in the GDT. In addition, rs-fMRI showed enhanced spontaneous neural activity in the postcentral gyrus and inferior parietal lobe in the SI group compared to the HC group.