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2017 ; 222
(2
): 669-706
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The functional logic of corticostriatal connections
#MMPMID27412682
Shipp S
Brain Struct Funct
2017[Mar]; 222
(2
): 669-706
PMID27412682
show ga
Unidirectional connections from the cortex to the matrix of the corpus striatum
initiate the cortico-basal ganglia (BG)-thalamocortical loop, thought to be
important in momentary action selection and in longer-term fine tuning of
behavioural repertoire; a discrete set of striatal compartments, striosomes, has
the complementary role of registering or anticipating reward that shapes
corticostriatal plasticity. Re-entrant signals traversing the cortico-BG loop
impact predominantly frontal cortices, conveyed through topographically ordered
output channels; by contrast, striatal input signals originate from a far broader
span of cortex, and are far more divergent in their termination. The term
'disclosed loop' is introduced to describe this organisation: a closed circuit
that is open to outside influence at the initial stage of cortical input. The
closed circuit component of corticostriatal afferents is newly dubbed
'operative', as it is proposed to establish the bid for action selection on the
part of an incipient cortical action plan; the broader set of converging
corticostriatal afferents is described as contextual. A corollary of this
proposal is that every unit of the striatal volume, including the long, C-shaped
tail of the caudate nucleus, should receive a mandatory component of operative
input, and hence include at least one area of BG-recipient cortex amongst the
sources of its corticostriatal afferents. Individual operative afferents contact
twin classes of GABAergic striatal projection neuron (SPN), distinguished by
their neurochemical character, and onward circuitry. This is the basis of the
classic direct and indirect pathway model of the cortico-BG loop. Each pathway
utilises a serial chain of inhibition, with two such links, or three, providing
positive and negative feedback, respectively. Operative co-activation of direct
and indirect SPNs is, therefore, pictured to simultaneously promote action, and
to restrain it. The balance of this rival activity is determined by the
contextual inputs, which summarise the external and internal sensory environment,
and the state of ongoing behavioural priorities. Notably, the distributed sources
of contextual convergence upon a striatal locus mirror the transcortical network
harnessed by the origin of the operative input to that locus, thereby capturing a
similar set of contingencies relevant to determining action. The disclosed loop
formulation of corticostriatal and subsequent BG loop circuitry, as advanced
here, refines the operating rationale of the classic model and allows the
integration of more recent anatomical and physiological data, some of which can
appear at variance with the classic model. Equally, it provides a lucid
functional context for continuing cellular studies of SPN biophysics and
mechanisms of synaptic plasticity.
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