Abstract
Anatomically distinct areas within the basal ganglia encode flexible- and stable-value memories for visual objects (Hikosaka et al., 2014), but an important question remains: do they receive inputs from the same or different brain areas or neurons? To answer this question, we first located flexible and stable value-coding areas in the caudate head (CDh) and caudate tail (CDt) of two rhesus macaque monkeys, and then injected different retrograde tracers into these areas of each monkey. We found that CDh and CDt received different inputs from several cortical and subcortical areas including temporal cortex, prefrontal cortex, cingulate cortex, amygdala, claustrum and thalamus. Superior temporal cortex and inferior temporal cortex projected to both CDh and CDt, with more CDt-projecting than CDh-projecting neurons. In superior temporal cortex and dorsal inferior temporal cortex, layers 3 and 5 projected to CDh while layers 3 and 6 projected to CDt. Prefrontal and cingulate cortex projected mostly to CDh bilaterally, less to CDt unilaterally. A cluster of neurons in the basolateral amygdala projected to CDt. Rostral-dorsal claustrum projected to CDh while caudal-ventral claustrum projected to CDt. Within the thalamus, different nuclei projected to either CDh or CDt. The medial centromedian nucleus and lateral parafascicular nucleus projected to CDt while the medial parafascicular nucleus projected to CDh. The inferior pulvinar and lateral dorsal nuclei projected to CDt. The ventral anterior and medial dorsal nuclei projected to CDh. We found little evidence of neurons projecting to both CDh and CDt across the brain. These data suggest that CDh and CDt can control separate functions using anatomically separate circuits. Understanding the roles of these striatal projections will be important for understanding how value memories are created and stored.
Highlights
The caudate nucleus (CD) is involved in a variety of behaviors including voluntary movements, procedural learning and automatic behavior
Our previous data showed that two parallel pathways through the CD in the monkey contribute to reward-based learning, but in different ways (Kim and Hikosaka, 2013): the caudate head (CDh) encodes flexible values of visual objects based on short-term memories, while the caudate tail (CDt) encodes stable values of visual objects based on long-term memories
To help answer this question, we examined the anatomical inputs into distinct parts of the caudate by injecting retrograde neuronal tracers into CDh and CDt of two monkeys
Summary
The caudate nucleus (CD) is involved in a variety of behaviors including voluntary movements, procedural learning and automatic behavior (skill or habit; Jog et al, 1999; Miyachi et al, 2002; Samejima et al, 2005; Ding and Gold, 2012; Hikosaka et al, 2017). One of the first studies revealed that the CD receives topographical projections from the closest cortical regions, i.e., the frontal cortex (FC) projects to head, the parietal cortex (PC) projects to the body, and the temporal and occipital cortices project to the tail (Kemp and Powell, 1970) This model was later updated to show that multiple cortical areas project to the caudate in a topographic manner while other cortical regions send diffuse, non-topographic projections to the caudate (Selemon and Goldman-Rakic, 1985; Saint-Cyr et al, 1990). Do individual cortical neurons project to both CDh and CDt? Do projections to CDh and CDt arise from anatomically intermingled or distinct subpopulations of cortical neurons?
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