Multiple modes of hippocampal-prefrontal interactions in memory-guided behavior.

paper Cited Public

Authors: Shin, Justin D; Jadhav, Shantanu P
Year: 2016
Journal: Current opinion in neurobiology
PMID: 27543753
DOI: 10.1016/j.conb.2016.07.015
PMCID: PMC5056827

Figure 1

Distinct network states in the hippocampal-prefrontal network during behavior(a) Spike and local field potential (LFP) activity in CA1 region of the hippocampus (green) and PFC (black) as an animal approaches a reward well in a spatial task. From top to bottom, the plot shows respectively: broadband LFP (1–400 Hz) in CA1, ripple band filtered LFP (150–250 Hz) in CA1, raster plot with spikes from 18 CA1 place cells, broadband LFP in PFC, raster plot with spikes from 7 PFC neurons, and animal speed. As the animal runs on the track (speed scale bar: 10 cm/sec), CA1 place cells fire in a sequential order. (b) When the animal stops at the reward well, SWRs and replay activity are prominent in the hippocampus. Vertical gray rectangle backgrounds in a denote SWRs detected in CA1 LFP. (c) Theta oscillations are seen in hippocampus during running. Shaded area over CA1 LFP from a on an expanded time scale. Theta filtered LFP (6–12 Hz) is shown overlaid with the broadband LFP. Adapted from [31**] with permission from authors.

Figure 2

Theta and SWR interactions in the hippocampal-prefrontal network during behavior(a) Example of CA1 and PFC cells with overlapping spatial patterns of firing in a W-track spatial alternation task. Color scale indicates spiking intensity on the track. Both cells are preferentially active during outbound trajectories to right (arrows). (b) Schematic illustrating theta coupling between CA1 and PFC observed during exploratory behavior. Schematic on left illustrates phase-locking of spiking to theta oscillations; the one on right illustrates coherence, i.e. phase alignment of theta oscillations in CA1 and PFC. (c) CA1 and PFC cells are phase-locked to hippocampal theta at different characteristic phases. (d) Increase in CA1-PFC theta coherence specifically in the theta band (6–12 Hz) as animals approach the choice point in a maze. (e) Schematic illustrating replay of CA1 place cells during SWRs. Decoded CA1 activity represents spatial trajectories in the maze. SWRs are observed primarily at reward locations (cyan circles) on the W-maze. (f) Activity of CA1 and PFC cells aligned to hippocampal SWRs. PFC cells show both SWR-triggered activation and suppression of activity. (g) Reactivation of spatial information in the hippocampal-prefrontal network. CA1-PFC cell pairs with high spatial overlap are reactivated together during SWRs, while those with dissimilar patterns are suppressed. Adapted from [31**] with permission from authors.

Figure 3

Different network patterns can represent different modes of communication between brain regions. (a) Schematic illustrating that multiple network activity patterns mediate hippocampal-prefrontal interactions during memory-guided behavior. Theta interactions, associated with place cell activity in the hippocampus, are prominent as animals traverse locations in spatial mazes. Awake SWRs are associated with coordinated reactivation of ongoing experience in hippocampal-prefrontal ensembles. During SWRs, PFC cells with representations related to concurrently reactivated hippocampal cells are preferentially excited, while PFC cells with unrelated representations are inhibited. Gamma synchrony also mediates hippocampal-prefrontal interactions, and may play a role in organizing theta and SWR interactions. (b) A closed-loop feedback strategy that couples real-time detection to optogenetic perturbation can be used to selectively perturb communication during specific activity patterns (illustrated for SWRs).

#	Section	Preview
0	Introduction	The cognitive processes of learning, memory and decision making rely on neural circuits located in…
1	Introduction	The role of hippocampal - prefrontal interactions in cognition has been most clearly established in…
2	Introduction	Rhythmic oscillations at distinct frequencies, seen in the electroencephalogram or local field…
3	Introduction	We review evidence indicating that different network patterns represent multiple communication modes…
4	Multiple network patterns mediate hippocampal-prefrontal interactions	In the hippocampus, rapid, dynamic changes in network patterns are observed in the hippocampus…
5	Multiple network patterns mediate hippocampal-prefrontal interactions	These diverse anatomical connections between the regions can support bi-directional interactions…
6	Multiple network patterns mediate hippocampal-prefrontal interactions	Hippocampal-prefrontal interactions during theta oscillations are the most well-established, with…
7	Multiple network patterns mediate hippocampal-prefrontal interactions	Hippocampal SWRs represent another prominent network state associated with hippocampal-cortical…
8	Multiple network patterns mediate hippocampal-prefrontal interactions	to guide future actions, as well as planning [7,46,54,55]. Hippocampal replay during awake SWRs…
9	Multiple network patterns mediate hippocampal-prefrontal interactions	Another prominent rhythm, gamma oscillations, plays a role in local processing in both regions. In…
10	Multiple network patterns mediate hippocampal-prefrontal interactions	In addition to these three network patterns, other oscillations have also been proposed to play a…
11	What is the role of network patterns in memory-guided behavior?	There are some clues regarding the specific role of interactions during these different network…
12	What is the role of network patterns in memory-guided behavior?	whether ongoing PFC activity is aligned with these sequences during periods of high theta coherence…
13	What is the role of network patterns in memory-guided behavior?	In addition to theta, various findings suggest that coupling between regions during SWRs may have a…
14	What is the role of network patterns in memory-guided behavior?	The role of hippocampal-PFC gamma interactions in memory processes is still not clear and requires…
15	Linking network patterns and cognitive processes	Dissecting the roles of these diverse network patterns in cognition presents a significant…
16	Linking network patterns and cognitive processes	Simultaneous physiological monitoring in multiple regions will be necessary to further understand…
17	Linking network patterns and cognitive processes	Finally, interventional approaches with requisite temporal and spatial specificity must be utilized…
18	Summary	It has become increasingly clear that we must transition from approaching brain regions as modular…
19	Summary	prominent physiological patterns in these regions can reveal organizational principles through which…

Name	Type
4 Hz rhythms local	phenotype
animals	cohort
anterior cingulate cortex	anatomy
anxiety-like behavior	phenotype
awake SWRs local	phenotype
Awake SWRs local	phenotype
Behavioral history local	phenotype
Behavioral learning local	phenotype
beta oscillations	phenotype
Beta oscillations local	drug
CA1	anatomy
CA3	anatomy
cognition	phenotype
contextual memory retrieval local	phenotype
Correct trials	phenotype
cortex	anatomy
Cue-guided retrieval local	phenotype
Dorsal CA1 local	anatomy
Encoding local	phenotype
entorhinal cortex	anatomy
Fast gamma	phenotype
Flexibility local	phenotype
gamma oscillations	phenotype
Gamma oscillations local	drug
Gamma synchronization local	phenotype
gamma synchrony local	phenotype
Gamma synchrony local	phenotype
Hippocampal-PFC network local	anatomy
Hippocampal-prefrontal ensembles local	phenotype
hippocampal-prefrontal interaction local	phenotype
Hippocampal-prefrontal network	anatomy
Hippocampal SWR replay local	phenotype
hippocampus	anatomy
Imagination local	phenotype
Incorrect trials local	phenotype
infralimbic cortex	anatomy
Intermediate CA1 local	anatomy
learning	phenotype
long-term memory	phenotype
medial prefrontal cortex	anatomy
memory	phenotype
memory-guided behavior local	phenotype
Memory-guided behavior local	phenotype
Memory-guided decision making local	phenotype
memory-guided decisions local	phenotype
Network pattern local	phenotype
neurological disorders	phenotype
novelty detection	phenotype
Nucleus reuniens local	anatomy
optogenetic perturbation local	drug
Oscillatory coherence local	phenotype
perirhinal cortex	anatomy
Place cell activity local	phenotype
Place cell sequences local	phenotype
planning	phenotype
Postrhinal cortex local	anatomy
prefrontal cortex	anatomy
prelimbic cortex	anatomy
Prospective decision making local	phenotype
Reactivation local	phenotype
reinforcement learning	phenotype
retrieval	phenotype
reward	phenotype
sharp-wave ripples local	drug
Sharp-wave ripples local	drug
Sharp-wave ripples local	phenotype
Sharp wave-ripples (SWRs) local	phenotype
slow gamma	phenotype
slow-wave sleep	phenotype
Spatial cognitive maps local	phenotype
spatial learning	phenotype
spatial memory	phenotype
Spatial navigation	phenotype
Spiking correlations local	phenotype
subiculum	anatomy
SWR events local	phenotype
SWR replay local	phenotype
Task representations local	phenotype
temporal lobe	anatomy
theta band	phenotype
Theta coherence	phenotype
theta interactions local	phenotype
theta oscillations	phenotype
Theta synchrony local	phenotype
Ventral CA1 local	anatomy
ventral hippocampus	anatomy
Wakefulness	phenotype
working memory	phenotype

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