Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems

Abstract

Disconnection syndromes were originally conceptualized as a disruption of communication between different cerebral cortical areas. Two developments mandate a re-evaluation of this notion. First, we present a synopsis of our anatomical studies in monkey elucidating principles of organization of cerebral cortex. Efferent fibers emanate from every cortical area, and are directed with topographic precision via association fibers to ipsilateral cortical areas, commissural fibers to contralateral cerebral regions, striatal fibers to basal ganglia, and projection subcortical bundles to thalamus, brainstem and/or pontocerebellar system. We note that cortical areas can be defined by their patterns of subcortical and cortical connections. Second, we consider motor, cognitive and neuropsychiatric disorders in patients with lesions restricted to basal ganglia, thalamus, or cerebellum, and recognize that these lesions mimic deficits resulting from cortical lesions, with qualitative differences between the manifestations of lesions in functionally related areas of cortical and subcortical nodes. We consider these findings on the basis of anatomical observations from tract tracing studies in monkey, viewing them as disconnection syndromes reflecting loss of the contribution of subcortical nodes to the distributed neural circuits. We introduce a new theoretical framework for the distributed neural circuits, based on general, and specific, principles of anatomical organization, and on the architecture of the nodes that comprise these systems. We propose that neural architecture determines function, i.e., each architectonically distinct cortical and subcortical area contributes a unique transform, or computation, to information processing; anatomically precise and segregated connections between nodes define behavior; and association fiber tracts that link cerebral cortical areas with each other enable the cross-modal integration required for evolved complex behaviors. This model enables the formulation and testing of future hypotheses in investigations using evolving magnetic resonance imaging techniques in humans, and in clinical studies in patients with cortical and subcortical lesions.

O1‐05‐01: Frontotemporal dementia with the C9ORF72 hexanucleotide repeat expansion: Clinical, neuroanatomical and neuropathological features

“…The diffuse projections of these subcortical structures may account for the wide range of cognitive findings and cortical damage exhibited across the C9ORF72 mutation cohort here. Involvement of thalamus and cerebellar connections could underpin the prominent neuropsychiatric features shown by these cases (Andreasen et al, 1996;Schmahmann, 2005;Goossens et al, 2007;Straube et al, 2007;Schmahmann and Pandya, 2008;Tedesco et al, 2011), as well as episodic memory deficits ( Van der Werf et al, 2003;de Jong et al, 2008) somatic complaints, hallucinations and delusions (Kessler et al, 2009;Tedesco et al, 2011). Although none of our cases had frank cerebellar ataxia, this has been described in previous cases of chromosome 9 linked FTLD (Pearson et al, 2011).…”

“…We speculate that the relatively sparse cortical correlates shown in the voxel-based morphometry analysis of the C9ORF72 mutation cohort here may reflect wide inter-subject variation in cortical loss, with the more consistent involvement of subcortical grey matter structures (including thalamus and cerebellum) being a more robust signature of this mutation. We do not argue that the neuroanatomical signature of the C9ORF72 repeat expansion is restricted to these regions; subcortical structures typically act as hubs within structural and functional networks (Van der Werf et al, 2003;Schmahmann and Pandya, 2008;Tedesco et al, 2011), with projection targets that include other sites of pathological involvement (for example, the thalamus participates in a diencephalic network that also includes the hippocampi). The diffuse projections of these subcortical structures may account for the wide range of cognitive findings and cortical damage exhibited across the C9ORF72 mutation cohort here.…”

Language recovery and evidence of residual deficits after nonthalamic subcortical stroke: A 1 year follow-up study

“…These overall findings are in line with the idea that focal BG lesions are associated with impairments to functions of the same hemisphere (Schmahmann & Pandya, 2008). Indeed, lesions to the left BG mimic the lexical-semantic dysfunction typically observed after damage to the cortical regions involved in the left language network (Middleton & Strick, 2000), whereas lesions to the right BG impair the discourse and pragmatic aspects of language supported by the RH cortex that are crucial for social communication (Bookheimer, 2002).…”

Intelligence neurocircuitry: cortical and subcortical structures

“…Lesions of the ventral striatum nucleus lead to disinhibiting of behavior, irritation, addiction (reward circuit) and obsessive-compulsive disorder. Lesions in the putamen can lead to extrapyramidal syndrome symptoms, including akinesia and apathia (SCHMAHMANN and PANDYA, 2008).…”

“…In the posterior fossa syndrome (one type of cerebellar cognitive-affective syndrome) that occurs 48 hours after the excision of a cerebellar tumor, children show mutism, buccolingual apraxia, apathy and poor spontaneous movements. Emotional lability is evident with distraction, irritability and agitation (Figure 3) (SCHMAHMANN and PANDYA, 2008;PINAULT, 2004;HALASSA, CHEN, WIMMER et al, 2014;STOODLEY and SCHMAHMANN, 2010;VOOGD, 2003;CAHANA-AMITAY and ALBERT, 2014).…”