The Basal Ganglia and Chunking of Action Repertoires

“Motor representations specify ways of moving apt both for generating predictions about upcoming sensory consequences, and for construction of ever more sophisticated motor schemata via learning processes of ‘chunking’ and ‘parsing’ (Graybiel 1998).”

“Dopamine release during sequential ®nger movements in health and Parkinson's disease: a PET study Ines K. Goerendt,1 Cristina Messa,1,3,4,5 Andrew D. Lawrence,1,2 Paul M. Grasby,1 Paola Piccini1 and David J. Brooks1 1MRC Clinical Sciences Centre and Division of Neuroscience, Faculty of Medicine, Imperial College, Hamm…”

“The caudate/putamen (dorsal striatum) exhibits two distinct histological/histochemical compartments throughout its extent, divisible into island-like patches (containing striosomes; approximately 20% by volume) and an intervening matrix (containing matrisomes; 80%) everywhere else (Gerfen, 1985; Graybiel, 1998; Joel a…”

“Finally, long-term meditation affected the basal ganglia, which plays a role in rumination (Graybiel, 1998) and is thus of relevance to OCD (National Collaborating Centre for Mental Health, 2006).”

“The PFC seems to be related to learning and the basal ganglia to consolidation routines in automatic habits or procedures[22,23].”

“Hair-pulling and other kind of motoric habits can also be conceptualized as the inappropriate release of chunks of grooming behavior.(6) Hairpulling and other habits can be performed in a highly automatic fashion,(7) and trichotillomania is associated with impaired inhibition of motor responses.”

“Unique kinds of learning are associated with the basal ganglia (Graybiel, 1998; Knowlton, Mangels, & Squire, 1996); these include acquisition and execution of gestures that are compatible with processing of formulaic expressions.”

“Action chunking occurs after extensive training, involves a specific set of brain regions, and is thought to be essential for pursuing long-term goals and planning [5, 6].”

“We tested the wireless stimulation system in the striatum, an input nucleus of the basal ganglia implicated in important behavioral functions including voluntary movement (DeLong, 1990; Graybiel, 1998; Yin and Knowlton, 2006; Rossi and Yin, 2011).”

“The structure and function of BG output have received relatively little attention compared to the theory and experiments dealing with its internal circuitry (e.g., Frank 2011, Graybiel 1998, Klaus et al. 2019, Nelson & Kreitzer 2014), and thus we summarize work on the BG output pathways below.”

“PPD demonstrate an incomplete automatization of the sensorimotor integration process, forcing the system to continue to guide movement by sensory input (Graybiel, 1998).”

“They have been implicated in learning, habit formation, and reward (Graybiel, 1998; Yin and Knowlton, 2006), yet they also play a major role in motor control (DeLong et al.”

“This “pattern chunking” idea is allied to the notion of cortical or other higher-level pattern generators (Graybiel, 1998; Klein Breteler et al., 2007).”

“This beginning-and-end task-bracketing activity provided a compelling candidate neural correlate for the chunking of actions together into a habitual unit (Graybiel, 1998).”

“However, the striatum is also thought to compress the representation of temporally ordered motor and cognitive action sequences and to be involved in the performance of learned sequences (Jin, Tecuapetla, & Costa, 2014; Yin, 2010; Schubotz & von Cramon, 2002; Graybiel, 1998).”

“Striatosomes, discrete neuronal pools present in the ventral striatum, are mainly involved in the above-mentioned circuit through the direct pathway, whereas matrisomes interact with premotor and associative cortico-subcortical loops through the indirect pathway [18].”

“Corticol-basal ganglia circuits [1] have shown to be crucially involved in encoding of motor memories [34], probably guided by the rewardsensitive function of the dopamine-containing neurons in the substantia nigra [21].”

“These non-motor connections account, at least in part, for the involvement of the striatum in memory formation, mnemonic guidance of behavior and rewarding processes (Whishaw et al. 1987; Saint-Cyr et al. 1988; Knowlton et al. 1996; Graybiel 1998; Apicella et al. 1991).”

“The BG has been described as a region involved in sensorimotor coordination [Barn eoud, Descombris, Aubin, & Abrous, 2000; Lynd-Balta & Haber, 1994] and action selection [Graybiel, 1998; Jin & Costa, 2015], which requires integration of sensory information.”

“Neural circuitry in the basal ganglia (BG) is well known to be involved in the control of learned behaviors [5,6], and the striatum, the input structure of the BG, is well established as a key structure in the neural implementation of reinforcement learning [7-10].”

“In fact, Marsden and Obeso (1994) proposed a dual function of the basal ganglia: the first one would be to foster determined actions to support the creation of new routines, and the second to respond to unexpected circumstances in order to interrupt a sequence of actions to promote a novel action.”

“At a neurophysiological level, the cholinergic interneurons are thought to be the tonically active neurons (TANs) (Aosaki, Kimura, & Graybiel, 1995; Aosaki et al., 1994; Graybiel, 1995; Graybiel, 1998; Wilson, Chang, & Kitai, 1990).”

“DLS has long been associated with S-R behaviors (Graybiel, 1998; McDonald and White, 1993; Packard and Knowlton, 2002; Packard and McGaugh, 1996).”

“Moreover, because an intricately interconnected network of neurons is a property of cortical– basal ganglia circuitry in many animals (Graybiel, 1998; Kincaid et al., 1998; Bolam et al., 2000; Parent et al., 2000; Bar-Gad and Bergman, 2001), the capacity to preserve neuronal correlation across…”

“…features of Lab A. General context-reward association, like conditioned place preference, is an implicit Pavlovian process that is acquired more readily and with greater resistance to extinction than is the pairing of explicit, discrete stimuli with reward (Holland, 1992; Graybiel, 1998).”

“Much evidence suggests that the striatum is part of the habit-forming system of the mammalian brain, and that abnormal activation of striatal circuits occurs in disorders ranging from obsessive–compulsive (OC) disorder to addiction [1–4].”

“Other studies of basal ganglia function reveal its important role in configuring holistic and routinized gestures (Graybiel, 1998; Lieberman, 2002).”

“But why would silencing this region produce such an effect? With accrued experience, the DLS is posited to be a substrate for the concatenation of action sequence into a streamlined stimulus-driven response (Dezfouli et al., 2014; Graybiel, 1998; Jin and Costa, 2010).”

“However, given the sequential structure of these previous motor tasks, and given the additional role of the BG in assembling performance units from sequence elements (“chunking”) (Graybiel, 1998), impaired switching behavior in PD may result from both deficient chunking and updating.”

“This model draws on findings from studies of the basal ganglia, which suggest that these nuclei modulate procedural and configurational action programs (Mishkin, Malamut, and Bachevalier, 1984; Graybiel, 1998).”

“Graybiel AM (1998) The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 1, 119-136. Graybiel AM (2000) The basal ganglia. Curr. Biol. 14, R509-R511. Greengard P, PB Allen and AC Nairn (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23, 435-447. Grosshans…”

“This ‘‘beginning-and-end bracketing pattern’’ in DLS could represent the neural correlate for ‘‘chunking’’ multiple behavioral elements into a specific sequence (Graybiel, 1998; Smith and Graybiel, 2014).”

“The fact that neurons within the reward circuitry represent action, and sometimes action sequences, as well as reward (Graybiel, 1998; Hikosaka et al., 1989, 1999; Lavoie and Mizumori, 1994; Mulder et al., 2004; Schmitzer-Torbert and Redish, 2004; Schultz et al., 1997; van der Meer et al., 2010;…”

“, Noble, K., and Higgins, G. A. (2011). Impulsive action induced by amphetamine, cocaine and MK801 is reduced by 5-HT(2C) receptor”

“Graybiel (1997, 1998) proposed that the basal ganglia control the execution of the selected response through the use of thalamocortical loops and brainstem networks.”

“…in the processing of concatenated sequences in both beat-based timing (Grahn, 2009; Grahn & Rowe, 2009; H. Mer-chant, Grahn, Trainor, Rohrmeier, & Fitch, 2015; Teki, Grube, Kumar, & Griffiths, 2011) and chunking (Dahms et al., 2020; Graybiel, 1998; Wymbs, Bassett, Mucha, Porter, & Grafton, 2012).”

“The striatum is the main input structure of the basal ganglia, a set of nuclei involved in the organization of thoughts and behavior (Cummings, 1993), and reinforcementbased learning (Graybiel, 1998).”

“…evidence suggest that the basal ganglia are centrally involved in the learning process that leads to habit formation or the acquisition of skilled behavior (McDonald and White, 1994; Graybiel, 1995, 1998; Salmon and Butters, 1995; Knowlton et al., 1996; White, 1997; White and McDonald, 2002).”

“Striatum and globus pallidus are central regions associated with action selection, planning, and modulation of ongoing action (Graybiel, 1998; Jin et al., 2014; Kim & Hikosaka, 2015; Markowitz et al., 2018).”

“Graybiel (1998) proposed that the basal ganglia contribute to S–”

“The connections of the dorsal and ventral striatum, and their functional significance, have been extensively reviewed (Graybiel 1998; Heimer et al. 1995; Zahm 1999, 2000).”

“Whereas matrix receives input from associative and sensorimotor cortex, striosomes receive innervation mainly from limbic areas (Graybiel, 1995, 1998).”

“…Available online 25 August 2004 A sessing the p consistent r nction in o e obtained e h in normal s ural learning i ed a group o up of major d concurrent d k similarly t t processing i te explici p © K 1 c [ d nce ntly of see e reumed ing of 0] 0 d bstract The striatum has been consistently…”

“Outside the context of interval timing, one proposed function of the DS is organizing the hierarchical structure of learned response sequences (Graybiel, 1998; Fujii and Graybiel, 2005; Jin et al., 2009; Jin and Costa, 2010), which is consistent with a direct relationship to interval timing.”

“While dopamine is known to play a crucial role in forming new action chunks (Graybiel, 1998; Jin and Costa, 2015), its role in the expression of previously learned action chunks is less clear.”

“A proposed function of the dorsal striatum is to encode short motor programs to be linked together in order to increase complexity of motor output (Yin, 2010) thereby preventing excessive computational demands on cortical structures (Graybiel, 1998).”

“This is supported by a significant interaction of treatment and quadrant (F(4,54) 15.”

“Response strategies are considered to rely on the projections from the sensory and motor cortices to the BG circuits issued from the dorso-lateral striatum (DLS) to select directions of movement, using reinforcement learning capabilities of the BG to learn which cue is to be followed at a given time [16, 17].”

“Alternatively, the neural architecture could provide a template for rearranging cortical information in the striatum, and for selecting coherent inputs from functionally related motor cortical areas that the striatal region implements leading to trigger firing of the striatal output targets in the pallidum and nigra (…”

“Detailed tract tracing studies in nonhuman primates also demonstrate that there are two types of projections from the dorsolateral prefrontal cortex (DLPFC) to the head of the striatum: focal, targeted projections, and diffuse, widespread projections (Eblen and Graybiel, 1995).”

“Moreover, reactions to cues can occur unconsciously (Childress et al., 2008; Graybiel, 1998), making it difficult for abstinent addicts to recognize, anticipate, or prevent relapse.”

“Although regional brain activity was not measured here, learning of discrete motor sequence tasks, such as our serial targeting task, may be more dependent on basal ganglia circuits (5,15) than the tasks used in the aforementioned work (22,30).”

“It is also telling the involvement of the motor component of the lenticular nuclei bilaterally: these are of course part of a cortico-subcorticalcortical network that regulates motor behavior (Graybiel, 1998) and that is dysfunctional in movement disorders (see review in Crittenden and Graybiel, 2011).”

“This may be due to the fact that basal ganglia, an important node in the neural network purportedly dysfunctional in dystonia, are called into action not only in sensorymotor control [6, 14], but also in a number of cognitive functions [9].”