Frequency-specific hippocampal-prefrontal interactions during associative learning

Brincat, Scott L.; Miller, Earl K.

doi:10.1038/nn.3954

Cited by 171 publications

(180 citation statements)

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“…Although LFP recordings in bilateral V1 only showed robust primary optogenetically evoked responses, we do not preclude that the presence of secondary responses like slow oscillations may contribute to BOLD responses. Moreover, Cg, a prefrontal cortical region implicated in memory (42) and learning (43), was also activated in our fMRI experiments. This result reinforces the role of dHP in cognitive functions.…”

Section: Discussionsupporting

confidence: 52%

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Chan

Leong

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The hippocampus, including the dorsal dentate gyrus (dDG), and cortex engage in bidirectional communication. We propose that low-frequency activity in hippocampal-cortical pathways contributes to brain-wide resting-state connectivity to integrate sensory information. Using optogenetic stimulation and brain-wide fMRI and resting-state fMRI (rsfMRI), we determined the large-scale effects of spatiotemporal-specific downstream propagation of hippocampal activity. Low-frequency (1 Hz), but not high-frequency (40 Hz), stimulation of dDG excitatory neurons evoked robust cortical and subcortical brain-wide fMRI responses. More importantly, it enhanced interhemispheric rsfMRI connectivity in various cortices and hippocampus. Subsequent local field potential recordings revealed an increase in slow oscillations in dorsal hippocampus and visual cortex, interhemispheric visual cortical connectivity, and hippocampal-cortical connectivity. Meanwhile, pharmacological inactivation of dDG neurons decreased interhemispheric rsfMRI connectivity. Functionally, visually evoked fMRI responses in visual regions also increased during and after low-frequency dDG stimulation. Together, our results indicate that low-frequency activity robustly propagates in the dorsal hippocampal-cortical pathway, drives interhemispheric cortical rsfMRI connectivity, and mediates visual processing.hippocampus | resting-state functional connectivity | optogenetic | fMRI | low frequency T he hippocampus (HP) plays a prominent role in central nervous system functions, particularly in episodic memory (1, 2) and spatial navigation (3, 4). The HP, including the dentate gyrus (DG), can evoke large-scale influences on cortical activity, because the HP receives convergent information from sensory and limbic cortices before sending reciprocal divergent projections to create a highly interactive corticohippocampal-cortical network. The HP, including DG, CA3, and CA1, and neocortex, are connected via the entorhinal cortex (EC) (5, 6), such that the dorsolateral-to-ventromedial projection that originates in the EC corresponds to a dorsoventral axis of termination in the HP (5). This anatomical topography suggests that a functional gradient could exist along the HP dorsoventral axis. Previous studies demonstrated that dorsal HP (dHP) and cortex are functionally integrated during sensory processing and memory consolidation (7-9). Specifically, dHP can integrate multimodal sensory information and process memory operations (7) using excitatory longrange projections (10). This process occurs over multiple brain circuits, but the role of dHP in complex networks, particularly its influence on brain-wide functional connectivity, is not well understood.Resting-state functional MRI (rsfMRI) (11-14) provides an invaluable, noninvasive imaging technique to map long-range, brain-wide functional connectivity networks based on the temporal coherence of infraslow (0.005-0.1 Hz) blood oxygen level dependent (BOLD) activity. The functional relevance of specific brain-wide networks in co...

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Section: Discussionsupporting

confidence: 52%

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Chan

Leong

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In primate prefrontal cortex (PFC), a functional analog of NCL, one study reports that prospective selectivity for long-term paired associates does not appear until the end of the delay period, whereas visual similarity is the only factor influencing selectivity in the sample period (13). All studies of association learning in primate PFC, however, consistently report that such selectivity shifts earlier in the trial as the monkeys learn the correct response (14)(15)(16)(17), eventually reaching the cue period, when the animal can first start to prepare its response. This is also a typical finding in other studies of the PFC, where choice-related activity and error trial effects get stronger throughout the delay, but are also present in the sample period (18)(19)(20).…”

Section: Discussionmentioning

confidence: 99%

“…Primate hippocampus is a key brain area for association learning, with frequent demonstrations of learning-related activity (27)(28)(29)(30). The PFC is intimately connected to the hippocampus, and prefrontal-hippocampal interactions seem to play a major role during association learning (17,31). In contrast, the NCL has no direct connections to the hippocampus or surrounding structures (26,32,33).…”

Section: Discussionmentioning

confidence: 99%

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Veit

Pidpruzhnykova

Nieder

2015

Proc. Natl. Acad. Sci. U.S.A.

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The ability to form associations between behaviorally relevant sensory stimuli is fundamental for goal-directed behaviors. We investigated neuronal activity in the telencephalic area nidopallium caudolaterale (NCL) while two crows (Corvus corone) performed a delayed association task. Whereas some paired associates were familiar to the crows, novel associations had to be learned and mapped to the same target stimuli within a single session. We found neurons that prospectively encoded the chosen test item during the delay for both familiar and newly learned associations. These neurons increased their selectivity during learning in parallel with the crows' increased behavioral performance. Thus, sustained activity in the NCL actively processes information for the upcoming behavioral choice. These data provide new insights into memory representations of behaviorally meaningful stimuli in birds, and how such representations are formed during learning. The findings suggest that the NCL plays a role in learning arbitrary associations, a cornerstone of corvids' remarkable behavioral flexibility and adaptability.association learning | crow | single-cell recordings | nidopallium caudolaterale | memory T he ability to form arbitrary associations between sensory stimuli is fundamental for many flexible goal-directed behaviors. Corvids exploit learned associations intensively when adapting their behavior to a changing environment (1, 2). For example, scrub jays learn to associate different foods with different degradation speeds as a component of their episodic-like memory during food-caching behavior (3). The neuronal basis of corvids' ability to learn arbitrary associations has never been investigated.The avian cognitive integration area nidopallium caudolaterale (NCL) is a good candidate to investigate learning-related changes in the representation of initially unknown stimuli, as they acquire behavioral meaning during association learning. We have recently demonstrated that single NCL neurons encode abstract behavioral rules, irrespective of the arbitrary, learned cues used to instruct the rule (4). Furthermore, pigeons with lesions of the NCL show deficits in a reversal learning task, indicating that the NCL is a crucial structure to flexibly adapt behavior based on feedback during learning (5). The NCL is the main pallial target of dopaminergic projections from the midbrain (6), and dopamine signaling in striatal and cortical structures is involved in learning and memory processes in birds, as in mammals (7).Here we investigate changes in the neuronal representation while associative learning links arbitrary visual items in memory. We trained two carrion crows on a delayed paired-association learning (DPA) task and recorded NCL neurons during the course of learning. The task design allowed us to compare neuronal responses during the mapping of highly familiar images onto test items, as well as to follow the emergence of associative signals in the same neurons while the crows learned to map novel sample images onto the ...

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“…In primates, evidence points to learning-related hippocampal-PFC interactions during working memory (Bähner et al, 2015) and declarative memory (Brincat & Miller, 2015), while psychiatric disorders, including schizophrenia, post-traumatic stress disorder, and depression are associated with disrupted PFC-hippocampal connectivity (Godsil et al, 2013). A benefit to investigating functional connectivity is the ability to corroborate non-invasive primate work with more invasive techniques in experimental animal models, e.g., phase locking and coherence analysis (Sigurdsson & Duvarci, 2016).…”

Section: Future Studiesmentioning

confidence: 99%

The role of working memory and declarative memory in trace conditioning

Connor

Gould

2016

Neurobiology of Learning and Memory

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Translational assays of cognition that are similarly implemented in both lower and higher-order species, such as rodents and primates, provide a means to reconcile preclinical modeling of psychiatric neuropathology and clinical research. To this end, Pavlovian conditioning has provided a useful tool for investigating cognitive processes in both lab animal models and humans. This review focuses on trace conditioning, a form of Pavlovian conditioning typified by the insertion of a temporal gap (i.e., trace interval) between presentations of a conditioned stimulus (CS) and an unconditioned stimulus (US). This review aims to discuss pre-clinical and clinical work investigating the mnemonic processes recruited for trace conditioning. Much work suggests that trace conditioning involves unique neurocognitive mechanisms to facilitate formation of trace memories in contrast to standard Pavlovian conditioning. For example, the hippocampus and prefrontal cortex (PFC) appear to play critical roles in trace conditioning. Moreover, cognitive mechanistic accounts in human studies suggest that working memory and declarative memory processes are engaged to facilitate formation of trace memories. The aim of this review is to integrate cognitive and neurobiological accounts of trace conditioning from preclinical and clinical studies to examine involvement of working and declarative memory.

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Frequency-specific hippocampal-prefrontal interactions during associative learning

Cited by 171 publications

References 64 publications

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

The role of working memory and declarative memory in trace conditioning

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