A dopaminergic reward prediction error signal shapes maternal behavior in mice

Xie, Yunyao; Huang, Longwen; Corona, Alberto; Pagliaro, Alexa H.; Shea, Stephen D.

doi:10.1016/j.neuron.2022.11.019

Cited by 24 publications

(38 citation statements)

References 64 publications

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“…5b). Consistent with preceding studies 5,6 , VTA DA neurons showed time-locked activity immediately after pup interaction (Fig. 5e).…”

Section: Ofc Facilitates Vtada Neurons During Pup Retrievalsupporting

confidence: 91%

“…A classical study suggests that VTA DA neurons play an essential role in maternal behaviours 45 , and more recent studies have uncovered the temporal dynamics of their neural activity during pup retrieval 5,6 . Our data demonstrate a functional link through which OFC neurons facilitate pup-retrieval-locked VTA DA activities only during the early stages of learning (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…5). Given that VTA DA neuron activities during pup retrieval are thought to encode a social reward prediction error 6 , one intriguing possibility is that some activities in the OFC, particularly those time-locked to anticipatory and interaction categories, may contribute to this process. If this is the case, how does the OFC lose influence on VTA DA activities at the LM stage when maternal behavioural learning is completed?…”

Section: Discussionmentioning

confidence: 99%

“…1) in the downstream neural circuit? As the dopamine (DA) neurons in the ventral tegmental area (VTA DA ) can be directly regulated by OFC 29 and critically guide maternal motivation toward infants 6 , we next aimed to characterize VTA DA neurons as a potential output of the OFC. We first confirmed the direct projections from OFC Rbp4 neurons to the VTA (Extended Data Fig.…”

Section: Ofc Facilitates Vtada Neurons During Pup Retrievalmentioning

confidence: 99%

“…Through viral tracing and manipulations, we functionally identify the submedius thalamus as a prominent presynaptic partner of the OFC that shapes pup-related representations. Optogenetic inactivation of OFC reduces the pup retrieval-related activities of midbrain dopamine neurons 5,6 that promote maternal behaviours. Collectively, these findings reveal a higher-order cognitive network that connects innately formed, pup-related integrated representation to the top-down control of motivation centers, thus enabling efficient maternal behavioural learning..…”

mentioning

confidence: 99%

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Dopamine Dynamics Underlying Alloparental Behavioral Acquisition Facilitated by Top-down Orbitofrontal Inputs in Female Mice

Tasaka

Hagihara

Irie

et al. 2023

Preprint

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Maternal behaviours, which are crucial for the survival of mammalian infants, can be learned. How the efficient acquisition of these behaviours is implemented at the neural circuitry level remains poorly understood. Although prevalent models of neural circuits for parental behaviours often assume the frontal cortical network as an integrator of infant-related sensory signals and a controller of decision-making and motivation, these ideas have not been functionally tested. As such, detailed input/output neural circuit organizations of the frontal cortex in relation to parental behaviours remain unknown. Here we show that the orbitofrontal cortex (OFC) promotes efficient learning of maternal behaviours in virgin female mice when they are co-housed with lactating mothers. Chronic microendoscopy in freely behaving animals reveals robust representations of pup-directed anticipatory activities and ongoing sequential motions of pup retrieval that are innately sculpted and largely unaffected by learning. Through viral tracing and manipulations, we functionally identify the submedius thalamus as a prominent presynaptic partner of the OFC that shapes pup-related representations. Optogenetic inactivation of OFC reduces the pup retrieval-related activities of midbrain dopamine neurons that promote maternal behaviours. Collectively, these findings reveal a higher-order cognitive network that connects innately formed, pup-related integrated representation to the top-down control of motivation centers, thus enabling efficient maternal behavioural learning.

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“…5b). Consistent with preceding studies 5,6 , VTA DA neurons showed time-locked activity immediately after pup interaction (Fig. 5e).…”

Section: Ofc Facilitates Vtada Neurons During Pup Retrievalsupporting

confidence: 91%