The hippocampus frequently replays memories of past experiences during sharp-wave ripple (SWR) events. These events can represent spatial trajectories extending from the animal’s current location to ...distant locations, suggesting a role in the evaluation of upcoming choices. While SWRs have been linked to learning and memory, the specific role of awake replay remains unclear. Here we show that there is greater coordinated neural activity during SWRs preceding correct, as compared to incorrect, trials in a spatial alternation task. As a result, the proportion of cell pairs coactive during SWRs was predictive of subsequent correct or incorrect responses on a trial-by-trial basis. This effect was seen specifically during early learning, when the hippocampus is essential for task performance. SWR activity preceding correct trials represented multiple trajectories that included both correct and incorrect options. These results suggest that reactivation during awake SWRs contributes to the evaluation of possible choices during memory-guided decision making.
► Greater SWR reactivation of past experience precedes correct decisions ► Increased reactivation is specifically seen during learning ► Possible future paths are reactivated most strongly ► Hippocampal reactivation is related to memory-guided decision making
How does the brain use past experience to make decisions? Singer et al. report that, during learning, stronger hippocampal replay predicts subsequent correct decisions. Their findings provide a link between replay and an internal exploration of possible options during decision making.
The replay of previously stored memories during hippocampal sharp wave ripples (SWRs) is thought to support both memory retrieval and consolidation in distributed hippocampal-neocortical circuits. ...Replay events consist of precisely timed sequences of spikes from CA3 and CA1 neurons that are coordinated both within and across hemispheres. The mechanism of this coordination is not understood. Here, we show that during SWRs in both awake and quiescent states there are transient increases in slow gamma (20-50 Hz) power and synchrony across dorsal CA3 and CA1 networks of both hemispheres. These gamma oscillations entrain CA3 and CA1 spiking. Moreover, during awake SWRs, higher levels of slow gamma synchrony are predictive of higher quality replay of past experiences. Our results indicate that CA3-CA1 gamma synchronization is a central component of awake memory replay and suggest that transient gamma synchronization serves as a clocking mechanism to enable coordinated memory reactivation across the hippocampal network.
► Gamma oscillations transiently increase during hippocampal sharp wave ripples ► Gamma is synchronous across CA3 and CA1 of both hemispheres ► CA3 and CA1 neurons are entrained by gamma during sharp wave ripples ► Gamma synchrony is predictive of high quality memory replay
Spatially distributed hippocampal neurons replay stored memories, a process thought to support memory consolidation and retrieval. Carr et al. show that synchronized gamma oscillations bind distributed cell assemblies together and coordinate memory replay across the hippocampal circuit in both hemispheres.
Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal-neocortical networks. Replay is present during both sleep and waking behavior, but although sleep ...replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here, we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was more robust when the rat had recently been in motion than during extended periods of quiescence. Our results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, UILJ, UKNU, UL, UM, UPUK
Cognitive faculties such as imagination, planning, and decision-making entail the ability to represent hypothetical experience. Crucially, animal behavior in natural settings implies that the brain ...can represent hypothetical future experience not only quickly but also constantly over time, as external events continually unfold. To determine how this is possible, we recorded neural activity in the hippocampus of rats navigating a maze with multiple spatial paths. We found neural activity encoding two possible future scenarios (two upcoming maze paths) in constant alternation at 8 Hz: one scenario per ∼125-ms cycle. Further, we found that the underlying dynamics of cycling (both inter- and intra-cycle dynamics) generalized across qualitatively different representational correlates (location and direction). Notably, cycling occurred across moving behaviors, including during running. These findings identify a general dynamic process capable of quickly and continually representing hypothetical experience, including that of multiple possible futures.
Display omitted
•Firing across hippocampal neurons can regularly “take turns” (cycle) every ∼125 ms•Cycle firing is seen at single-cell, cell-pair, and population levels•Cycle firing encodes hypothetical experience, including multiple possible futures•Cycle coding generalizes across representational correlates, implying common process
Imagination, planning, and decision-making require the ability to generate representations of hypothetical experience. Kay et. al. find that neurons in the rat hippocampus can represent alternative hypothetical scenarios both regularly and quickly (every ∼125 ms). Further, the underlying activity has a temporal structure that is equivalent across different representational correlates (location and direction), implying a common process.
Hippocampal information processing is often described as two-state, with a place cell state during movement and a reactivation state during stillness. Relatively little is known about how the network ...transitions between these different patterns of activity during exploration. Here we show that hippocampal network changes quickly and continuously as animals explore and become familiar with initially novel places. We measured the relationship between moment-by-moment changes in behavior and information flow through hippocampal output area CA1 in rats. We examined local field potential (LFP) patterns, evoked potentials and ensemble spiking and found evidence suggestive of a smooth transition from strong CA3 drive of CA1 activity at low speeds to entorhinal cortical drive of CA1 activity at higher speeds. These changes occurred with changes in behavior on a timescale of less than a second, suggesting a continuous modulation of information processing in the hippocampal circuit as a function of behavioral state.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The brain is a massive neuronal network, organized into anatomically distributed sub-circuits, with functionally relevant activity occurring at timescales ranging from milliseconds to years. Current ...methods to monitor neural activity, however, lack the necessary conjunction of anatomical spatial coverage, temporal resolution, and long-term stability to measure this distributed activity. Here we introduce a large-scale, multi-site, extracellular recording platform that integrates polymer electrodes with a modular stacking headstage design supporting up to 1,024 recording channels in freely behaving rats. This system can support months-long recordings from hundreds of well-isolated units across multiple brain regions. Moreover, these recordings are stable enough to track large numbers of single units for over a week. This platform enables large-scale electrophysiological interrogation of the fast dynamics and long-timescale evolution of anatomically distributed circuits, and thereby provides a new tool for understanding brain activity.
•Modular polymer electrode-based system capable of recording up to 1,024 channels•Recording from 375 single units across multiple regions in freely behaving rats•Single-unit recording longevity for 160 or more days post-implantation•System capable of tracking populations of single units continuously for over a week
Chung et al. present a large-scale, multi-site, polymer electrode-based recording platform. The modular system is capable of data collection from up to 1,024 channels in freely behaving rats, enabling long-term studies of distributed networks.
How does an animal know where it is when it stops moving? Hippocampal place cells fire at discrete locations as subjects traverse space, thereby providing an explicit neural code for current location ...during locomotion. In contrast, during awake immobility, the hippocampus is thought to be dominated by neural firing representing past and possible future experience. The question of whether and how the hippocampus constructs a representation of current location in the absence of locomotion has been unresolved. Here we report that a distinct population of hippocampal neurons, located in the CA2 subregion, signals current location during immobility, and does so in association with a previously unidentified hippocampus-wide network pattern. In addition, signalling of location persists into brief periods of desynchronization prevalent in slow-wave sleep. The hippocampus thus generates a distinct representation of current location during immobility, pointing to mnemonic processing specific to experience occurring in the absence of locomotion.
Apolipoprotein (apo) E4 is the major genetic risk factor for Alzheimer’s disease (AD), but the mechanism by which it causes cognitive decline is unclear. In knockin (KI) mice, human apoE4 causes ...age-dependent learning and memory impairments and degeneration of GABAergic interneurons in the hippocampal dentate gyrus. Here we report two functional apoE4-KI phenotypes involving sharp-wave ripples (SWRs), hippocampal network events critical for memory processes. Aged apoE4-KI mice had fewer SWRs than apoE3-KI mice and significantly reduced slow gamma activity during SWRs. Elimination of apoE4 in GABAergic interneurons, which prevents learning and memory impairments, rescued SWR-associated slow gamma activity but not SWR abundance in aged mice. SWR abundance was reduced similarly in young and aged apoE4-KI mice; however, the full SWR-associated slow gamma deficit emerged only in aged apoE4-KI mice. These results suggest that progressive decline of interneuron-enabled slow gamma activity during SWRs critically contributes to apoE4-mediated learning and memory impairments.
Display omitted
•ApoE4-KI mice show age-dependent attenuation of slow gamma activity during SWRs•ApoE4-KI mice, both young and aged, have fewer SWRs than apoE3-KI mice•ApoE4-induced slow gamma impairment, not SWR abundance, is interneuron dependent•Progressive slow gamma dysfunction during SWRs may contribute to cognitive decline
Gillespie et al. show that Alzheimer’s disease risk factor apoE4 alters hippocampal sharp-wave ripples (SWRs), network events important for memory function. In particular, dysfunction of SWR-associated slow gamma activity may critically contribute to apoE4-induced learning and memory impairment.
During development, activity-dependent processes increase the specificity of neural responses to stimuli, but the role that this type of process plays in adult plasticity is unclear. We examined the ...dynamics of hippocampal activity as animals learned about new environments to understand how neural selectivity changes with experience. Hippocampal principal neurons fire when the animal is located in a particular subregion of its environment, and in any given environment the hippocampal representation is sparse: less than half of the neurons in areas CA1 and CA3 are active whereas the rest are essentially silent. Here we show that different dynamics govern the evolution of this sparsity in CA1 and upstream area CA3. CA1, but not CA3, produces twice as many spikes in novel compared with familiar environments. This high rate firing continues during sharp wave ripple events in a subsequent rest period. The overall CA1 population rate declines and the number of active cells decreases as the environment becomes familiar and task performance improves, but the decline in rate is not uniform across neurons. Instead, the activity of cells with initial peak spatial rates above approximately 12 Hz is enhanced, whereas the activity of cells with lower initial peak rates is suppressed. The result of these changes is that the active CA1 population comes to consist of a relatively small group of cells with strong spatial tuning. This process is not evident in CA3, indicating that a region-specific and long timescale process operates in CA1 to create a sparse, spatially informative population of neurons.
Regions within the prefrontal cortex are thought to process beliefs about the world, but little is known about the circuit dynamics underlying the formation and modification of these beliefs. Using a ...task that permits dissociation between the activity encoding an animal's internal state and that encoding aspects of behavior, we found that transient increases in the volatility of activity in the rat medial prefrontal cortex accompany periods when an animal's belief is modified after an environmental change. Activity across the majority of sampled neurons underwent marked, abrupt, and coordinated changes when prior belief was abandoned in favor of exploration of alternative strategies. These dynamics reflect network switches to a state of instability, which diminishes over the period of exploration as new stable representations are formed.
PDF
