Environment-based object values learned by local network in the striatum tail

Abstract

Basal ganglia contribute to object-value learning, which is critical for survival. The underlying neuronal mechanism is the association of each object with its rewarding outcome. However, object values may change in different environments and we then need to choose different objects accordingly. The mechanism of this environment-based value learning is unknown. To address this question, we created an environment-based value task in which the value of each object was reversed depending on the two scene-environments (X and Y). After experiencing this task repeatedly, the monkeys became able to switch the choice of object when the scene-environment changed unexpectedly. When we blocked the inhibitory input from fast-spiking interneurons (FSIs) to medium spiny projection neurons (MSNs) in the striatum tail by locally injecting IEM-1460, the monkeys became unable to learn scene-selective object values. We then studied the mechanism of the FSI-MSN connection. Before and during this learning, FSIs responded to the scenes selectively, but were insensitive to object values. In contrast, MSNs became able to discriminate the objects (i.e., stronger response to good objects), but this occurred clearly in one of the two scenes (X or Y). This was caused by the scene-selective inhibition by FSI. As a whole, MSNs were divided into two groups that were sensitive to object values in scene X or in scene Y. These data indicate that the local network of striatum tail controls the learning of object values that are selective to the scene-environment. This mechanism may support our flexible switching behavior in various environments.

Neuronal mechanism of the encoding of socially familiar faces in the striatum tail

“…After the monkeys fully recovered from surgery, we started training them in the oculomotor tasks. Several procedures, including the surgery, behavioral task, and statistical analysis, were identical between this and our previous studies (5,42) .…”

“…We defined the putamen tail as the region 0-3.5 mm from the ventral edge of the putamen and the cdPUT as the region above it (Kunimatsu et al, 2019;Kunimatsu et al, 2021). Because the putamen tail and CDt share the same anatomical pathway (10,12) and showed similar long-term value coding in a previous study (5), we combined neurons in these areas as STRt neurons.…”

Lateral Habenula Responses During Eye Contact in a Reward Conditioning Task

“…SC is a well-studied brain area that projects to OPN ( Yoshida et al, 2001 ; Takahashi et al, 2005 ) and the premotor burst neurons that control eye movements ( Sugiuchi et al, 2005 ; Izawa et al, 2007 ; Takahashi et al, 2014 ). Moreover, the basal ganglia-SC pathway is critical to modulating automatic skills and habitual eye movements established by reward history ( Kim et al, 2015 ; Amita and Hikosaka, 2019 ; Kunimatsu et al, 2021 ). LHb neurons access the basal ganglia-SC loop at the level of striatum and dopamine neurons and are thus well-positioned to modulate emotional factors driving learning in oculomotor behavior ( Figure 4 ) ( Matsumoto and Hikosaka, 2007 ; Hong and Hikosaka, 2013 ).…”

Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques

“…In real life, different objects are typically found in different environments. Thus, the act of encountering a new environment itself conveys predictive information about what objects are likely to be found therein and accordingly influences behavior 5 – 7 . How does the brain process such predictive environmental information?…”