The functional logic of corticostriatal connections

Abstract

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.

Synchronized activation of striatal direct and indirect pathways underlies the behavior in unilateral dopamine‐depleted mice

“…The reasons for the differences in neuronal recruitment between patterned and continuous stimulation, although interesting, are not the focus of this paper; methodological aspects perhaps involving a ChR2‐activated calcium conductance; reciprocal multisynaptic influences between direct and indirect SPNs and motor cortex (Burke et al., ; Freeze, Kravitz, Hammack, Berke, & Kreitzer, ; O'Hare et al., ; Oldenburg & Sabatini, ; Shipp, ), intrastriatal influences on SPNs (Planert, Szydlowski, Hjorth, Grillner, & Silberberg, ; Taverna, Ilijic, & Surmeier, ) and or the participation of interneurons (Damodaran, Evans, & Blackwell, ; Dehorter et al., ) should be considered in further analyses. Modulation of neuronal assemblies by specific patterns of neuronal stimulation may represent a modified animal model to study the pathogenesis in basal ganglia.…”

“…The reasons for the differences in neuronal recruitment between patterned and continuous stimulation, although interesting, are not the focus of this paper; methodological aspects perhaps involving a ChR2-activated calcium conductance; reciprocal multisynaptic influences between direct and indirect SPNs and motor cortex (Burke et al, 2017;Freeze, Kravitz, Hammack, Berke, & Kreitzer, 2013;O'Hare et al, 2016;Oldenburg & Sabatini, 2015;Shipp, 2017), intrastriatal F I G U R E 7 Analysis of network dynamics of D1 and D2 SPNs. The similarity index matrices of the stimulation induced by continuous (a) and stimulation in patterned pulses (b) show that continuous delivery of light activated sets of neurons with higher similarity index across stimulations, than stimulation delivered in patterned pulses.…”

Laminar fMRI: Applications for cognitive neuroscience

“…Together, these examples demonstrate how laminar fMRI can be utilized to better characterize the nature of feedback effects from high-level respectively. The pulvinar is frequently implicated in attention, and shares feedforward and feedback connections with many regions throughout cortex (Shipp, 2003). This led Gouws et al…”

“…This hypothesis can be tested using laminar fMRI, with the prediction that positive modulations originate in dorsolateral pulvinar, which projects primarily layers III and IV of occipital cortex (Shipp, 2003), while negative modulations originate in dorsomedial pulvinar, which projects primarily to parietal cortex (Behrens et al, 2003;Gutierrez et al, 2000)and then to feedback layers of visual cortex. Interestingly, one recent study found that increased neuronal firing rates from spatial attention were significantly stronger in input layer IV of macaque V4 compared to other layers (Nandy, Nassi, & Reynolds, 2017), providing some support for this hypothesis.…”

Danckert & Isacescu fMRI of boredom replication

“…When bored, people were willing to pay more for music -as though desperate for any stimulation to escape the boredom. Activity in the caudate nucleus -a subcortical structure known to be important for representing reward value [33] -was associated with decisions to avoid the boring task. Activity in the insula cortex was associated with just how willing people were to pay to avoid boredom -the higher your willingness to pay to avoid boredom the more activity was seen in the insula [32].…”