Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum

By Suzanne N. Haber, Julie L. Fudge, Nikolaus R. McFarland. Journal of Neuroscience, 2000

1,562 citations recorded by the source corpus.

Clinical manifestations in diseases affecting the dopamine system include deficits in emotional, cognitive, and motor function. Although the parallel organization of specific corticostriatal pathways is well documented, mechanisms by which dopamine might integrate information across different cortical/basal ganglia circuits are less well understood. We analyzed a collection of retrograde and anterograde tracing studies to understand how the striatonigrostriatal (SNS) subcircuit directs information flow between ventromedial (limbic), central (associative), and dorsolateral (motor) striatal regions. When viewed as a whole, the ventromedial striatum projects to a wide range of the dopamine cells and receives a relatively small dopamine input. In contrast, the dorsolateral striatum (DLS) receives input from a broad expanse of dopamine cells and has a confined input to the substantia nigra (SN). The central striatum (CS) receives input from and projects to a relatively wide range of the SN. The SNS projection from each striatal region contains three substantia nigra components: a dorsal group of nigrostriatal projecting cells, a central region containing both nigrostriatal projecting cells and its reciprocal striatonigral terminal fields, and a ventral region that receives a specific striatonigral projection but does not contain its reciprocal nigrostriatal projection. Examination of results from multiple tracing experiments simultaneously demonstrates an interface between different striatal regions via the midbrain dopamine cells that forms an ascending spiral between regions. The shell influences the core, the core influences the central striatum, and the central striatum influences the dorsolateral striatum. This anatomical arrangement creates a hierarchy of information flow and provides an anatomical basis for the limbic/cognitive/motor interface via the ventral midbrain.

Subfields: Cellular and Molecular Neuroscience, Neurology

View Paper: https://www.semanticscholar.org/paper/e0d67d44de66779452fbf9152662993df4247fd9

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Citations in the corpus

Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling (2011, background): “Anatomical analysis in rodents and nonhuman primates suggests that the midbrain and striatal components of the mesocorticolimbic DA system are connected in a spiraling manner (Haber et al., 2000; Ikemoto, 2007).”
Goals and Habits in the Brain (2013, neutral): “One influential proposal is that a protracted exposure to addictive drugs recruits dopamine-dependent striato-nigro-striatal ascending spirals (Haber et al., 2000; Joel and Weiner, 2000) from the nucleus accumbens to more dorsal regions of the striatum (Everitt et al., 2008).”
Psychology of Habit. (2016, background): “Though anatomically separate, the two loops can interact, for example, through spiraling dopaminergic connectivity (Haber et al. 2000).”
Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli (2011, neutral): “…may correspond to a transition from limbic and prefrontal cortical control over goal-directed behavior to dorsostriatal control as drug intake becomes compulsive (Haber et al., 2000; Kalivas and Volkow, 2005; Everitt and Robbins, 2005; Everitt et al., 2008; Hyman et al., 2006; Ikemoto, 2007).”
Actor-critic models of the basal ganglia: new anatomical and computational perspectives (2002, methodology): “As a result of this organization, the limbic striatum reciprocates its DA input and innervates DA neurons projecting to the associative (mainly caudate nucleus) and motor striatum; the associative striatum reciprocates part of its DA input and innervates DA neurons projecting to the motor striatum, ”
Striatal plasticity and basal ganglia circuit function (2008, background): “In more complex schemes, these circuits are integrated within an ascending hierarchy of open, interconnected loops emerging from limbic cortex and ventral striatum into associative and motor regions (Haber et al., 2000; Joel and Weiner, 1994; Parent, 1990).”
Human Reinforcement Learning Subdivides Structured Action Spaces by Learning Effector-Specific Values (2009, background): “The basis for this assumption is the relatively coarse organization of the ascending dopaminergic projection (Haber et al., 2000), in which relatively few dopamine neurons innervate a very large territory of forebrain (Schultz, 1998; Matsuda et al., 2009).”
Anticipatory affect: neural correlates and consequences for choice (2008, neutral): “Thus, the NAcc projects to the MPFC via the thalamus, which then directly projects back to the medial caudate, which then back to more dorsal regions of the prefrontal cortex via the thalamus, and so forth (Haber et al. 2000; Ferris et al. 2004; Lehericy et al. 2004; Draganski et al. 2008).”
Imaging dopamine receptors in humans with [11C]-(+)-PHNO: Dissection of D3 signal and anatomy (2011, background): “…boundary of VST was defined so as to include NAC, medial CD, rostroventral PU and also to be consistent with the functional anatomy of VST as defined in connectivity studies (Parent and Hazrati, 1995; Haber and McFarland, 1999; Haber et al., 2000; Cohen et al., 2009; Haber and Knutson, 2009).”
Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits (2015, background): “This information notably enriches the ascending spiral model proposed by Haber et al. (2000), which could not make definitive statements about striatal inputs onto DAergic versus non-DAergic midbrain cells.”
Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards (2007, background): “These areas project to very different neural target”
Impulsivity, compulsivity, and top-down cognitive control. (2011, neutral): “…control may be implemented: from the Il-PFC or the hippocampus to the shell, from the PL-PFC to the core and by currently unspeciﬁed interactions between the core and shell regions, either directly or indirectly via ‘‘spiralling cascades’’ of striato-VTA-striatal circuitry (Haber et al., 2000).”
Stereotypic behaviour in captive animals: fundamentals and implications for welfare and beyond. (2006, background): “They influence each other (e.g. Kalivas and Nakamura, 1999; Rolls, 1999; Haber et al., 2000; Haber, 2003), something little touched on in this volume (though see Chapter 8).”