Involvement of Striatal Direct Pathway in Visual Spatial Attention in Mice
Lupeng Wang, Richard J. Krauzlis
Abstract
The basal ganglia are implicated in a range of perceptual functions [1Ding L. Gold J.I. The basal ganglia’s contributions to perceptual decision making.Neuron. 2013; 79: 640-649Abstract Full Text Full Text PDF PubMed Scopus (103) Google Scholar], in addition to their well-known role in the regulation of movement [2Park J. Coddington L.T. Dudman J.T. Basal Ganglia Circuits for Action Specification.Annu. Rev. Neurosci. 2020; 43: 485-507Crossref PubMed Scopus (19) Google Scholar]. One unifying explanation for these diverse roles is that the basal ganglia control the level of commitment to particular motor or cognitive outcomes based on the behavioral context [3Thura D. Cisek P. The Basal Ganglia Do Not Select Reach Targets but Control the Urgency of Commitment.Neuron. 2017; 95: 1160-1170Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar, 4Turner R.S. Desmurget M. Basal ganglia contributions to motor control: a vigorous tutor.Curr. Opin. Neurobiol. 2010; 20: 704-716Crossref PubMed Scopus (253) Google Scholar]. If this explanation is applicable to the allocation of visual spatial attention, then the involvement of basal ganglia circuits should incorporate the subject’s expectations about the spatial location of upcoming events as well as the routing of visual signals that guide the response. From the viewpoint of signal detection theory, these changes in the level of commitment might correspond to shifts in the subject’s decision criterion, one of two distinct components recently ascribed to visual selective attention [5Luo T.Z. Maunsell J.H.R. Attention can be subdivided into neurobiological components corresponding to distinct behavioral effects.Proc. Natl. Acad. Sci. USA. 2019; 116: 26187-26194Crossref Scopus (11) Google Scholar]. We tested this idea using unilateral optogenetic activation of neurons in the dorsal striatum of mice during a visual spatial attention task [6Wang L. Krauzlis R.J. Visual Selective Attention in Mice.Curr. Biol. 2018; 28: 676-685Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar], taking advantage of the ability to specifically target medium spiny neurons in the “direct” pathway associated with promoting responses [7Vicente A.M. Galvão-Ferreira P. Tecuapetla F. Costa R.M. Direct and indirect dorsolateral striatum pathways reinforce different action strategies.Curr. Biol. 2016; 26: R267-R269Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar, 8Kravitz A.V. Freeze B.S. Parker P.R.L. Kay K. Thwin M.T. Deisseroth K. Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry.Nature. 2010; 466: 622-626Crossref PubMed Scopus (1189) Google Scholar]. By comparing results across attention task conditions, we found that direct-pathway activation caused changes in performance determined by the spatial probability and location of the visual event. Moreover, across conditions with identical visual stimulation, activation shifted the decision criterion selectively when attention was directed to the contralateral visual field. These results demonstrate that activity through the basal ganglia may play an important and distinct role among the multifarious mechanisms that accomplish visual spatial attention.