A primate temporal cortex–zona incerta pathway for novelty seeking

Ogasawara, Takaya; Sogukpinar, Fatih; Zhang, Kaining; Feng, Yangyang; Pai, Julia; Jezzini, Ahmad; Monosov, Ilya E.

doi:10.1038/s41593-021-00950-1

Cited by 43 publications

(32 citation statements)

References 131 publications

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“…The latter approach provides higher flexibility to arbitrate between different policies and is hence more compatible with the rapid change of behavior observed in our human participants that is triggered by the reward value they find in episode 1 (Fig. 5B1-2 and Supplementary Materials); this approach is also more consistent with experimental evidence for partially separate neural pathways of noveltyand reward-induced behaviors 19,65,72–75 . Moreover, our 3rd observation shows that the relative importance of different policies is regulated by the degree of reward optimism – in line with the known influence of environmental variables on the preference for novelty 41,42,74 and curiosity-driven behavior 76,77 .…”

Section: Discussionsupporting

confidence: 83%

“…However, there are multiple distinct theoretical models to describe directed exploration 5,12,25,[61][62][63] , and it has been debated which one is best suited to explain human behavior. Here, we focused on the class of intrinsically motivated RL algorithms and designed an experimental paradigm that enabled us to dissociate predictions of three main models of intrinsic motivation in neuroscience 13,18,19,64,65 and psychology 16,17,66,67 . Our 1st and 2nd observations above support noveltydriven RL algorithms as models of human curiosity-driven exploration even in situations where seeking novelty is not optimal for exploration -visible as a persistent distraction by rewardindependent stochasticity.…”

Section: Discussionmentioning

confidence: 99%

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The curse of optimism: a persistent distraction by novelty

Modirshanechi

Lin

et al. 2022

Preprint

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Human curiosity has been interpreted as a drive for exploration and modeled by intrinsically motivated reinforcement learning algorithms. An unresolved challenge in machine learning is that these algorithms are prone to distraction by reward-independent stochastic stimuli. We ask whether humans exhibit the same distraction pattern in their behavior as the algorithms. To answer this question, we design a multi-step decision-making paradigm containing an unknown number of states in a stochastic part of the environment, combined with a reward-manipulation that varies optimism of participants regarding the availability of rewards. We show that (i) participants exhibit a persistent distraction by novelty in the stochastic part; (ii) reward optimism increases this distraction; and (iii) the persistent distraction is consistent with the predictions of algorithms driven by novelty but not with ‘optimal’ algorithms driven by information-gain. Our results suggest that humans use sup-optimal but computationally cheap curiosity-driven policies for exploration in complex environments.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

The curse of optimism: a persistent distraction by novelty

Modirshanechi

Lin

et al. 2022

Preprint

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“…Few studies have directly examined connections of the ZI in nonhuman primates. The studies that have focused on ZI connections identified specific motor and sensory connections to the central or caudal ZI [53, 54, 55, 56, 89, 91–95]. Additional cortical inputs have been noted from the anterior and posterior cingulate cortices and from the anterior, ventromedial temporal cortex [56, 96–98].…”

Section: Discussionmentioning

confidence: 99%

“…The studies that have focused on ZI connections identified specific motor and sensory connections to the central or caudal ZI [53, 54, 55, 56, 89, 91–95]. Additional cortical inputs have been noted from the anterior and posterior cingulate cortices and from the anterior, ventromedial temporal cortex [56, 96–98]. Subcortical connections include: PAG, superior colliculus, interstitial nucleus of Cajal, pontine nuclei superior colliculus, interstitial nucleus of Cajal, pontine nuclei (PAG), and the spinal cord [99–103].…”

Section: Discussionmentioning

confidence: 99%

“…The nonhuman primate (NHP) ZI is also divided into four regions, the anterior pole/rostral region (ZIr), the ZId, ZIv and a caudal region (ZIc). Similar to rodents, the ZIv and ZIc are linked to sensory and motor systems [22,[53][54][55] and plays a role in novelty seeking [56]. However, little is known about PFC/ACC inputs to the ZI or how its connections intersect with BG circuits.…”

Section: Introductionmentioning

confidence: 99%

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The rostral zona incerta: a subcortical integrative hub and potential DBS target for OCD

Haber

Lehman

Maffei

et al. 2022

Preprint

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Background: The zona incerta (ZI) is involved in mediating survival behaviors and is connected to a wide range of cortical and subcortical structures, including key basal ganglia nuclei. Based on these connections and their links to behavioral modulation, we propose the ZI is a connectional hub for mediating between top-down and bottom-up control and a possible target for deep brain stimulation for obsessive compulsive disorder. Methods: We analyzed the trajectory of cortical fibers to the ZI in nonhuman and human primates, based on tracer injections in monkeys and high-resolution diffusion MRI in humans. The organization of cortical and subcortical connections with the ZI were identified in the nonhuman primate studies. Results: Monkey anatomic data and human dMRI data showed a similar trajectory of fibers/streamlines to the ZI. PFC/ACC terminals all converge within the rostral ZI (ZIr), with dorsal and lateral areas most prominent. Motor areas terminate caudally. Dense subcortical reciprocal connections included the thalamus, medial hypothalamus, substantia nigra/ventral tegmental area, reticular formation, and pedunculopontine nucleus and a dense nonreciprocal projection to the lateral habenula (LHb). Additional connections included amygdala, dorsal raphe nucleus, and periaqueductal grey. Conclusions: Dense connections with dorsal and lateral PFC/ACC cognitive control areas and LHb and SN/VTA coupled with inputs from the amygdala, hypothalamus, and brainstem, suggests that the ZIr is a subcortical hub positioned to modulate between top-down and bottom-up control. A DBS electrode placed in the ZIr would involve both connections common to other DBS sites, but also would capture several critically distinctive connections.

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Identification of a Hippocampus‐to‐Zona Incerta Projection involved in Motor Learning

Zhang,

Wang,

Peng

et al. 2024

Advanced Science

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Motor learning (ML), which plays a fundamental role in growth and physical rehabilitation, involves different stages of learning and memory processes through different brain regions. However, the neural mechanisms that underlie ML are not sufficiently understood. Here, a previously unreported neuronal projection from the dorsal hippocampus (dHPC) to the zona incerta (ZI) involved in the regulation of ML behaviors is identified. Using recombinant adeno‐associated virus, the projections to the ZI are surprisingly identified as originating from the dorsal dentate gyrus (DG) and CA1 subregions of the dHPC. Furthermore, projection‐specific chemogenetic and optogenetic manipulation reveals that the projections from the dorsal CA1 to the ZI play key roles in the acquisition and consolidation of ML behaviors, whereas the projections from the dorsal DG to the ZI mediate the retrieval/retention of ML behaviors. The results reveal new projections from the dorsal DG and dorsal CA1 to the ZI involved in the regulation of ML and provide insight into the stages over which this regulation occurs.

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A primate temporal cortex–zona incerta pathway for novelty seeking

Cited by 43 publications

References 131 publications

The curse of optimism: a persistent distraction by novelty

The curse of optimism: a persistent distraction by novelty

The rostral zona incerta: a subcortical integrative hub and potential DBS target for OCD

Identification of a Hippocampus‐to‐Zona Incerta Projection involved in Motor Learning

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