Anatomical and Functional Comparison of the Caudate Tail in Primates and the Tail of the Striatum in Rodents: Implications for Sensory Information Processing and Habitual Behavior

Lee, K. W.; An, Soo-Youn; Park, Jun; Lee, S. H.; Kim, Hyoung F.

doi:10.14348/molcells.2023.0051

Cited by 7 publications

(7 citation statements)

References 69 publications

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“…In addition, the tail striatum receives input primarily from sensory cortices, contrasting with the dorsolateral striatum, which receives predominantly motor cortex input. The primary inputs to the rodent tail striatum are the visual and auditory cortex, and this input is selective for specific divisions, with the auditory cortex selectively innervating the intermediate division (Hunnicutt et al., 2016; Lee et al., 2023; Miyamoto et al., 2018). We now show functional division in the tail striatum, confirming that the divisions are both anatomically and functionally distinct.…”

Section: Discussionmentioning

confidence: 99%

“…The tail striatum's unique organisation into divisions and role as a sensory processing region is conserved between species. A corresponding region, the caudate tail, is present in primates, including humans (Lee et al., 2023; Valjent & Gangarossa, 2021). The caudate tail has been implicated in sensory symptoms of Parkinson's disease, such as hallucinations, which 75% of people experience over the disease course (Weil & Reeves, 2020).…”

Section: Discussionmentioning

confidence: 99%

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Dopamine transmission in the tail striatum: Regional variation and contribution of dopamine clearance mechanisms

Riley,

Gould,

Lloyd

et al. 2024

Journal of Neurochemistry

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The striatum can be divided into four anatomically and functionally distinct domains: the dorsolateral, dorsomedial, ventral and the more recently identified caudolateral (tail) striatum. Dopamine transmission in these striatal domains underlies many important behaviours, yet little is known about this phenomenon in the tail striatum. Furthermore, the tail is divided anatomically into four divisions (dorsal, medial, intermediate and lateral) based on the profile of D1 and D2 dopamine receptor‐expressing medium spiny neurons, something that is not seen elsewhere in the striatum. Considering this organisation, how dopamine transmission occurs in the tail striatum is of great interest. We recorded evoked dopamine release in the four tail divisions, with comparison to the dorsolateral striatum, using fast‐scan cyclic voltammetry in rat brain slices. Contributions of clearance mechanisms were investigated using dopamine transporter knockout (DAT‐KO) rats, pharmacological transporter inhibitors and dextran. Evoked dopamine release in all tail divisions was smaller in amplitude than in the dorsolateral striatum and, importantly, regional variation was observed: dorsolateral ≈ lateral > medial > dorsal ≈ intermediate. Release amplitudes in the lateral division were 300% of that in the intermediate division, which also exhibited uniquely slow peak dopamine clearance velocity. Dopamine clearance in the intermediate division was most dependent on DAT, and no alternative dopamine transporters investigated (organic cation transporter‐3, norepinephrine transporter and serotonin transporter) contributed significantly to dopamine clearance in any tail division. Our findings confirm that the tail striatum is not only a distinct dopamine domain but also that each tail division has unique dopamine transmission characteristics. This supports that the divisions are not only anatomically but also functionally distinct. How this segregation relates to the overall function of the tail striatum, particularly the processing of multisensory information, is yet to be determined.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Dopamine transmission in the tail striatum: Regional variation and contribution of dopamine clearance mechanisms

Riley,

Gould,

Lloyd

et al. 2024

Journal of Neurochemistry

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“…Various types of values can originate from sensory input such as tactile and visual sensations. The basal ganglia (BG) might process values from these diverse sensory inputs because neurons in the cortical regions that process each type of sensory information innervate structures in the BG system [1][2][3] . Interestingly, the number of neurons is known to decrease as information flows from the cortex to each successive structure in the BG [4][5][6] .…”

Section: Introductionmentioning

confidence: 99%

“…To complete tasks involving visual stimuli, structures in the BG system, including the putamen and caudate, process the value information [16][17][18][19] . Notably, the putamen in the BG system anatomically receives input from the somatosensory cortex, including finger regions, and from midbrain dopamine neurons for value encoding 3,20,21 . That suggests a plausible role for the putamen in processing value information about tactile stimuli perceived through the fingers.…”

Section: Introductionmentioning

confidence: 99%

Efficient value encoding through convergence of tactile and visual value information in the primate putamen

Hwang,

Park,

Lee

et al. 2024

Preprint

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The processing of diverse sensory values by a limited number of basal ganglia neurons raises the question of whether each value is processed independently or combined as the number of neurons decreases from the cortex to downstream structures. Here, we discovered that tactile and visual values were partially converged in the primate putamen, enhancing its efficiency in encoding values while preserving modality information. Humans and monkeys performed tactile and visual value discrimination tasks. Notably, the human putamen selectively represented both tactile and visual values in fMRI scans. Single-unit electrophysiology further revealed that half of the individual neurons in the macaque putamen encoded both tactile and visual values, and the other half encoded each value separately. The bimodal value neurons enable more efficient value encoding using fewer neurons than the modality-selective value neurons. Our data suggest that the basal ganglia system uses modality convergence to efficiently encode values with limited resources.

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“…Furthermore, recent research in macaque monkeys revealed that goal-directed and habitual behavior are guided through distinct regions of the basal ganglia along the rostral-caudal axis, rather than the medial-lateral axis. For example, the rostral portion of the caudate (caudate head) is selectively involved in the reversal task, whereas the caudal part (caudate tail) plays a role in habitual behavior (2,(16)(17)(18). These findings motivate the exploration of various primate striatal regions, considering their distinct characteristics compared to rodents, in the context of cognitive flexibility.…”

Section: Introductionmentioning

confidence: 99%

Distinct representation of cognitive flexibility and habitual stability in the primate putamen, caudate, and ventral striatum

An,

Hwang,

Lee

et al. 2024

Preprint

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Recent primate studies have demonstrated a functional distinction along the rostral—caudal axis of the striatum, which has challenged the conventional view that flexible adaptation and habitual action differ in processing along the medial—lateral axis. We found that neurons in the rostral putamen, caudate, and ventral striatum encode values flexibly updated for adaptive choices, rather than values stably sustained for visual habit. In the reversal value learning, rostral striatal neurons dynamically updated their value discrimination responses after value reversals, whereas, in the stable value retrieval, most did not encode the value. Notably, caudate neurons were faster to update values after reversal trials than ventral striatum neurons. Slow-learning neurons were identified selectively in the ventral striatum. In each trial, their learning speeds were similar during initial learning, suggesting a parallel value update in each striatal region. Our findings thus indicate that the rostral striatum prioritizes cognitive flexibility over habitual stability.

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Anatomical and Functional Comparison of the Caudate Tail in Primates and the Tail of the Striatum in Rodents: Implications for Sensory Information Processing and Habitual Behavior

Cited by 7 publications

References 69 publications

Dopamine transmission in the tail striatum: Regional variation and contribution of dopamine clearance mechanisms

Dopamine transmission in the tail striatum: Regional variation and contribution of dopamine clearance mechanisms

Efficient value encoding through convergence of tactile and visual value information in the primate putamen

Distinct representation of cognitive flexibility and habitual stability in the primate putamen, caudate, and ventral striatum

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