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7 The CM/PF as a Target for Neurosurgical Interventions in Brain Disorders

7 The CM/PF as a Target for Neurosurgical Interventions in Brain Disorders

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of the CM/Pf-striatal system in attention, set-shifting, and cognitive flexibility is

highly significant because these functions are impaired in neurodegenerative diseases

that affect the basal ganglia, particularly PD and HD. The fact that CM/Pf neurons

undergo massive degeneration in these diseases further supports this possibility.

Future studies aimed at dissecting out the respective role of the CM-putamen versus

Pf-caudate nucleus in cognition, and the involvement of these networks in cognitive

impairments associated with PD are warranted. On a therapeutic perspective, additional knowledge about the cellular and molecular properties of CM/Pf neurons that

make them particularly sensitive to neurodegeneration must be gained, so that potential protective or neurorestorative therapies can be considered.

Acknowledgments This work was supported by grants from the National Institutes of Health to

YS and TW (R01 NS083386; P50NS071669) and the NIH infrastructure grant to the Yerkes

National Primate Research Center (P51 OD011132).



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Chapter 5



Dopamine and Its Actions in the Basal Ganglia

System

Daniel Bullock



5.1



Introduction: Consensus Summary of Dopamine’s

Actions in the Circuitry of the Basal Ganglia



There have been many recent excellent reviews of selected aspects of the dopamine

(DA) system, including the range of stimuli and internal signals to which DA neurons respond (e.g., Bromberg-Martin et al. 2010; Schultz 2013), how DA release

depends jointly on DA neuron firing and myriad factors present at release sites in

the basal ganglia (BG) (e.g., Rice et al. 2011), the systematic effects of DA in the

striatum (e.g., Gerfen and Surmeier 2011), and the role dopamine plays in various

neurological disorders (e.g., Linnet 2014; Lloyd et al. 2014; Covey et al. 2014;

Belujon and Grace 2015; Nutt et al. 2015) beyond its critical role in Parkinson’s

disease and schizophrenia (e.g., Iversen and Iversen 2007). This chapter will reprise

many of the key findings needed to understand the consensus that is emerging about

the neural systems—especially the BG system—within which DA plays its most

critical role.

Like noradrenaline (NA), dopamine (DA) is an aminergic neurotransmitter, and

Dahlström and Fuxe (1964) identified and designated 14 clusters of aminergic neurons: A1–A7 designate NA clusters, and A8–A14 designate DA clusters, most in the

midbrain (see also Björklund and Dunnett 2007). In each cluster, DA cells are mixed

with other cell types, but in all of these clusters, the aminergic neurons represent a

large proportion of cells, and they typically project aminergic axons far beyond the

nuclei in which their somas reside. Other brain structures also contain intermixed



D. Bullock, Ph.D. (*)

Department of Psychological and Brain Sciences, Boston University,

677 Beacon Street, Boston, MA 02215, USA

e-mail: danb@bu.edu

© Springer International Publishing Switzerland 2016

J.-J. Soghomonian (ed.), The Basal Ganglia, Innovations in Cognitive

Neuroscience, DOI 10.1007/978-3-319-42743-0_5



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DA neurons—a good example is the retina—but these neurons are not a large proportion of the total, and function as interneurons, with no projections beyond the

area. Recently, Fuxe and colleagues (2010) reviewed the huge literature that has

developed since the A8–A14 clusters were mapped. They reprised impressive evidence that (1) a highly similar mapping applies across a wide range of mammalian

species and (2) DA often works via volume transmission, which utilizes diffusion

well beyond release sites (Rice and Cragg 2008; but see Ishikawa et al. 2013), hence

does not require that the DA release sites be immediately adjacent to the receptors

at which DA acts. Of course, all systemically delivered neuroactive drugs also work

via volume transmission, after crossing the blood–brain barrier. Consistent with this

mode of operation, single DA neurons exhibit remarkably widespread branching,

with multiple axonal bushes, in target areas such as the striatum (e.g., Matsuda et al

2009). Thus, DA is typically regarded as a nonspecific, “broadcast” signal, highly

distinct from the specific, topographically organized projections found in other neural systems, e.g., at successive stages of processing within a sensory modality, or in

the motor output pathways.

Although DA signals play diverse roles in the neural symphony, one prototypical

and vital role is as a primary mediator of the ancient learning process by which

animals explore novel environments and thereby learn both to choose actions that

are expected to lead to more rewarding outcomes, and to suppress actions expected

to lead to less rewarding or aversive outcomes. Dopamine strongly affects such

learning via its systematic effects on LTD and LTP of glutamatergic synapses

between afferents to striatum and the medium spiny neurons (MSPNs) that project

from striatum to other BG nuclei. However, DA also has strong effects on performance, including both motor and cognitive performance. Its influence on performance is powerfully attested by the tight link between striatal DA loss and

Parkinsonian akinesia, but it is also revealed in much subtler ways, such as a higher

velocity of eye movements to rewarded than to equidistant but non-rewarded targets

(Hong and Hikosaka 2011), and altered reaction time distributions following sleep

deprivation, which have been reproduced in a computational model that includes

dopamine–adenosine interactions in striatum (Bullock and St. Hilaire 2014).

Action selection based on expected outcomes is enabled by mammalian forebrain circuits, among which the striatum and other constituents of the BG (see

Fig. 5.1) have a preeminent status (Swanson 2005; Gurney et al. 2015). Although

DA innervation is densest in striatum, it also reaches many other parts of the brain,

especially parts of the BG, thalamus, and cerebral cortex. Moreover, the innervation

of cerebral cortex is significantly more elaborated in primates than in rodents (Smith

et al. 2014). Because operation of the BG is so critically dependent on dense innervation from DA neurons of cluster A10 (much of which falls in the VTA), A9

(mostly in the SNc), and A8 (mostly in the retrorubral area = RRA), these pools are

regarded as an integral part of the BG system in this chapter. Thus, the BG system

spans cells found in both the subcortical forebrain and the midbrain.

DA acts differentially in striatum by facilitating a “direct”, action-promoting

pathway, and by simultaneously dis-facilitating an “indirect”, action-opposing path-



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