Marielena Sosa
Profile Url: marielena-sosa
Researcher at Kavli Institute for Fundamental Neuroscience, UCSF
Cell, 2020-01-30
Cognitive faculties such as imagination, planning, and decision-making entail the ability to project into the future. Crucially, animal behavior in natural settings implies that the brain can generate representations of future scenarios not only quickly but also constantly over time, as external events continually unfold. Despite this insight, how the brain accomplishes this remains unknown. Here we report neural activity in the hippocampus encoding two future scenarios (two upcoming maze paths) in constant alternation at 8 Hz: one scenario per 8 Hz cycle (125 ms). We further found that the underlying cycling dynamic generalized across multiple hippocampal representations (location and direction) relevant to future behavior. These findings identify an extremely fast and regular dynamical process capable of representing future possibilities.
Neuron, 2019-12-18
Memories of positive experiences require the brain to link places, events, and reward outcomes. Neural processing underlying the association of spatial experiences with reward is thought to depend on interactions between the hippocampus and the nucleus accumbens (NAc)1-9. Hippocampal projections to the NAc arise from both the ventral hippocampus (vH) and the dorsal hippocampus (dH)6-12, and studies using optogenetic interventions have demonstrated that either vH5,6 or dH7 input to the NAc can support behaviors dependent on spatial-reward associations. It remains unclear, however, whether dH, vH, or both coordinate memory processing of spatial-reward information in the hippocampal-NAc circuit under normal conditions. Times of memory reactivation within and outside the hippocampus are marked by hippocampal sharp-wave ripples (SWRs)13-19, discrete events which facilitate investigation of inter-regional information processing. It is unknown whether dH and vH SWRs act in concert or separately to engage NAc neuronal networks, and whether either dH or vH SWRs are preferentially linked to spatial-reward representations. Here we show that dH and vH SWRs occur asynchronously in the awake state and that NAc spatial-reward representations are selectively activated during dH SWRs. We performed simultaneous extracellular recordings in the dH, vH, and NAc of rats learning and performing an appetitive spatial task and during sleep. We found that individual NAc neurons activated during SWRs from one subdivision of the hippocampus were typically suppressed or unmodulated during SWRs from the other. NAc neurons activated during dH versus vH SWRs showed markedly different task-related firing patterns. Only dH SWR-activated neurons were tuned to similarities across spatial paths and past reward, indicating a specialization for the dH-NAc, but not vH-NAc, network in linking reward to discrete spatial paths. These temporally and anatomically separable hippocampal-NAc interactions suggest that dH and vH coordinate opposing channels of mnemonic processing in the NAc.
Humans have the ability to retrieve memories with various degrees of specificity, and recent advances in reinforcement learning have identified benefits to learning when past experience is represented at different levels of temporal abstraction. How this flexibility might be implemented in the brain remains unclear. We analyzed the temporal organization of rat hippocampal population spiking to identify potential substrates for temporally flexible representations. We examined activity both during locomotion and during memory-retrieval-associated population events known as sharp wave-ripples (SWRs). We found that spiking during SWRs is rhythmically organized with higher event-to-event variability than spiking during locomotion-associated population events. Decoding analyses using clusterless methods further suggest that similar spatial experience can be replayed in multiple SWRs, each time with a different rhythmic structure whose periodicity is sampled from a lognormal distribution. This variability is preserved despite the decline in SWR rates that occurs as environments become more familiar: in more familiar environments the width of the lognormal distribution increases, further enhancing the range of temporal variability. We hypothesize that the variability in temporal organization of hippocampal spiking provides a mechanism for retrieving remembered experiences with various degrees of specificity. ### Competing Interest Statement The authors have declared no competing interest.
Representations of past and possible future experiences play a critical role in memory and decision-making processes. The hippocampus expresses these types of representations during sharp-wave ripple (SWR) events, and previous work identified a minority of SWRs that contain "replay" of spatial trajectories at ~20x real-world speeds. Efforts to understand replay typically make multiple assumptions about which events to examine and what sorts of representations constitute replay. We therefore lack a clear understanding of both the prevalence and the range of representational dynamics associated with replay. Here we develop a state space model that uses a combination of movement dynamics of different speeds to capture the spatial content and time evolution of replay during SWRs. Using this model, we find that the large majority of replay events contain spatially coherent, interpretable content. Furthermore, most events progress at real-world, rather than accelerated, movement speeds, consistent with actual experiences. ### Competing Interest Statement The authors have declared no competing interest.