Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making

Symanski, Claire A.; Bladon, John; Kullberg, Emi T.; Jadhav, Shantanu P.

doi:10.1101/2020.06.08.140939

Cited by 9 publications

(14 citation statements)

References 116 publications

(180 reference statements)

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“…In adult mice, olfactory sampling has been reported to induce firing and augment the synchrony within LEC-HP-PFC networks [34][35][36][37][38]42]. Even in anesthetized neonatal mice, odor exposure led to an increase in beta band activity in LEC [43].…”

Section: Pfc Pathwaymentioning

confidence: 99%

“…Moreover, synchronized beta oscillations between OB-HP and LEC-HP are critically involved in odor learning (Igarashi et al, 2014;Martin et al, 2007Martin et al, , 2006Ravel et al, 2003). Recently, beta oscillations in prefrontal-hippocampal networks have been identified to support the utilization of odor cues for memory-guided decision making (Symanski et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

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Olfactory-driven beta band entrainment of limbic circuitry during neonatal development

Kostka

Hanganu‐Opatz

2021

Preprint

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Cognitive processing relies on the functional refinement of the limbic circuitry during the first two weeks of life. During this developmental period, when most sensory systems are still immature, the sense of olfaction acts as 'door to the world', providing the main source of environmental inputs. However, it is unknown whether early olfactory processing shapes the development of the limbic circuitry. Here, we address this question by combining simultaneous in vivo recordings from the olfactory bulb (OB), lateral entorhinal cortex (LEC), hippocampus (HP), and prefrontal cortex (PFC) with opto- and chemogenetic manipulations of mitral/tufted cells (M/TCs) in the OB of non-anesthetized neonatal mice. We show that the neonatal OB synchronizes the limbic circuity in beta frequency range. Moreover, it drives neuronal and network activity in LEC, as well as subsequently, HP and PFC via long-range projections from mitral cells (MCs) to HP-projecting LEC neurons. Thus, OB activity controls the communications within limbic circuits during neonatal development.

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Section: Pfc Pathwaymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Olfactory-driven beta band entrainment of limbic circuitry during neonatal development

Kostka

Hanganu‐Opatz

2021

Preprint

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“…Although less studied, there is also evidence that beta rhythms (15-30 Hz) synchronize hippocampal memory networks (Martin, Beshel and Kay, 2007; Igarashi et al ., 2014; Allen et al ., 2016; Symanski et al ., 2022). In rats, beta is often seen in the hippocampus during odor-based memory tasks and has also been associated with long-term odor memory (Martin, Beshel and Kay, 2007) and temporal contexts (Allen et al ., 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Notably, beta is also found in the olfactory bulb but is lost there when centrifugal inputs are cut off (Martin, Beshel and Kay, 2007). Olfactory bulb-hippocampal coherence is not clearly related to memory and decision making but may develop in parallel (Symanski et al ., 2022). Further, hippocampal beta is low early in learning and higher when memory is stable and engaged in a flexible manner (Martin, Beshel and Kay, 2007; Igarashi et al ., 2014; Allen et al ., 2016).…”

Section: Introductionmentioning

confidence: 99%

Reuniens transiently synchronizes memory networks at beta frequencies

Jayachandran

Viena

Garcia

et al. 2022

Preprint

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Using episodic memories to help guide decisions requires top-down medial prefrontal cortex interactions with the hippocampus. Mechanistically, this integrated prefrontal-hippocampal memory state is thought to be organized by synchronized network oscillations and mediated by connectivity with the nucleus reuniens of the thalamus. Here, we recorded local field potentials from the prefrontal-reuniens-hippocampal network while rats were engaged in a nonspatial sequence memory task which helps isolate memory-related activity from running-related oscillations. We found that synchronous prefrontal-hippocampal beta bursts (15-30 Hz) were dominant during memory trials, whereas synchronous theta (6-12 Hz) was highest during running. Beta rose during a trial and peaked just before a decision, whereas theta was highest during running. Beta bursts first appeared in reuniens and then in prefrontal and hippocampal sites simultaneously, suggesting beta could be directly driven by reuniens. To test this, we used an optogenetic approach (retroAAV-ChR2) to see if reuniens was capable of driving prefrontal-hippocampal beta synchrony. Reuniens activation induced prefrontal-hippocampal beta coherence, and reduced theta coherence, resembling the observed memory-driven network state. These findings demonstrate for the first time that reuniens contributes to memory by driving transient synchronous beta in the prefrontal-hippocampal system facilitating coherent interactions that sub-serve memory-based decision making.

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“…In adult rodents, coherent beta oscillations between OB and brain areas such as PIR, LEC, hippocampus, and prefrontal cortex have been implicated in memory processing and decision making ( Martin et al, 2006 , 2007 ; Igarashi et al, 2014 ; Symanski et al, 2021 ). Interestingly, the generation of beta oscillations in OB has been shown to depend on centrifugal inputs ( Neville and Haberly, 2003 ; Ravel et al, 2003 ).…”

Section: Discussionmentioning

confidence: 99%

Postnatal Development of Centrifugal Inputs to the Olfactory Bulb

Kostka

Bitzenhofer

2022

Front. Neurosci.

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Processing in primary sensory areas is influenced by centrifugal inputs from higher brain areas, providing information about behavioral state, attention, or context. Activity in the olfactory bulb (OB), the first central processing stage of olfactory information, is dynamically modulated by direct projections from a variety of areas in adult mice. Despite the early onset of olfactory sensation compared to other senses, the development of centrifugal inputs to the OB remains largely unknown. Using retrograde tracing across development, we show that centrifugal projections to the OB are established during the postnatal period in an area-specific manner. While feedback projections from the piriform cortex (PIR) are already present shortly after birth, they strongly increase in number during postnatal development with an anterior-posterior gradient. Contralateral projections from the anterior olfactory nucleus (AON) are present at birth but only appeared postnatally for the nucleus of the lateral olfactory tract (nLOT). Numbers of OB projecting neurons from the lateral entorhinal cortex (LEC), ventral hippocampus, and cortical amygdala (CoA) show a sudden increase at the beginning of the second postnatal week and a delayed development compared to more anterior areas. These anatomical data suggest that limited top-down influence on odor processing in the OB may be present at birth, but strongly increases during postnatal development and is only fully established later in life.

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Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making

Cited by 9 publications

References 116 publications

Olfactory-driven beta band entrainment of limbic circuitry during neonatal development

Olfactory-driven beta band entrainment of limbic circuitry during neonatal development

Reuniens transiently synchronizes memory networks at beta frequencies

Postnatal Development of Centrifugal Inputs to the Olfactory Bulb

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