What and Where Information in the Caudate Tail Guides Saccades to Visual Objects

Abstract

We understand the world by making saccadic eye movements to various objects. However, it is unclear how a saccade can be aimed at a particular object, because two kinds of visual information, what the object is and where it is, are processed separately in the dorsal and ventral visual cortical pathways. Here we provide evidence suggesting that a basal ganglia circuit through the tail of the monkey caudate nucleus (CDt) guides such object-directed saccades. First, many CDt neurons responded to visual objects depending on where and what the objects were. Second, electrical stimulation in the CDt induced saccades whose directions matched the preferred directions of neurons at the stimulation site. Third, many CDt neurons increased their activity before saccades directed to the neurons’ preferred objects and directions in a free-viewing condition. Our results suggest that CDt neurons receive both ‘what’ and ‘where’ information and guide saccades to visual objects.

Visual Information Shapes the Dynamics of Corticobasal Ganglia Pathways during Response Selection and Inhibition

“…In accord with anatomical and neurophysiological evidence, visual information within the ventral stream projected into the BG whereas the dorsal stream was connected with both the BG and pFC (Kravitz et al, 2013). In both humans and primates, the ventral pathway (including FFA and LOC) has been reported to carry detailed stimulus information into the striatum, whereas the dorsal stream (including parietal cortex and PO) links to the striatum and further relates information into pFC (Yamamoto, Monosov, Yasuda, & Hikosaka, 2012;Saint-Cyr, Ungerleider, & Desimone, 1990). Our results comply and extend these reports by specifying how information is integrated into the BG to select an overt response.…”

Basal Ganglia Circuits for Reward Value–Guided Behavior

“…Indeed, the CD has a strong access to oculomotor mechanisms. First, electrical stimulation of the CDh and CDb (Kitama et al 1991; Watanabe & Munoz 2011) as well as CDt (Yamamoto et al 2012) facilitates the initiation of saccades. CDh-CDb stimulation also suppresses saccades (Watanabe & Munoz 2010).…”

Value-driven attentional priority signals in human basal ganglia and visual cortex

“…In the case of visual selection, such habitual responding has been linked to the tail of the caudate nucleus. Neurons in the caudate tail represent both the identity and position of visual objects (Yamamoto et al, 2012), and these representations are strengthened by associative reward learning (Yamamoto et al, 2013). Stimulating neurons in the caudate tail can initiate a saccade (Yamamoto et al, 2012), and saccades are known to be guided by attentional priority signals (Hoffman & Subramaniam, 1995; Thompson & Bichot, 2005).…”

“…Neurons in the caudate tail represent both the identity and position of visual objects (Yamamoto et al, 2012), and these representations are strengthened by associative reward learning (Yamamoto et al, 2013). Stimulating neurons in the caudate tail can initiate a saccade (Yamamoto et al, 2012), and saccades are known to be guided by attentional priority signals (Hoffman & Subramaniam, 1995; Thompson & Bichot, 2005). The role of the caudate tail in mediating involuntary attentional capture is not known, however, and whether the representation of stimuli in the caudate tail can be modulated by reward learning in humans has not been tested.…”