Sequential activation of neurons that occurs during “offline” states, such as sleep or awake rest, is correlated with neural sequences recorded during preceding exploration phases. This so-called reactivation, or replay, has been observed in a number of different brain regions such as the striatum, prefrontal cortex, primary visual cortex and, most prominently, the hippocampus. Reactivation largely co-occurs together with hippocampal sharp-waves/ripples, brief high-frequency bursts in the local field potential. Here, we first review the mounting evidence for the hypothesis that reactivation is the neural mechanism for memory consolidation during sleep. We then discuss recent results that suggest that offline sequential activity in the waking state might not be simple repetitions of previously experienced sequences. Some offline sequential activity occurs before animals are exposed to a novel environment for the first time, and some sequences activated offline correspond to trajectories never experienced by the animal. We propose a conceptual framework for the dynamics of offline sequential activity that can parsimoniously describe a broad spectrum of experimental results. These results point to a potentially broader role of offline sequential activity in cognitive functions such as maintenance of spatial representation, learning, or planning.

The hippocampal network produces sequences of neural activity even when there is no time-varying external drive. In offline states, the temporal sequence in which place cells fire spikes correlates with the sequence of their place fields. Recent experiments found this correlation even between offline sequential activity (OSA) recorded before the animal ran in a novel environment and the place fields in that environment. This preplay phenomenon suggests that OSA is generated intrinsically in the hippocampal network, and not established by external sensory inputs. Previous studies showed that continuous attractor networks with asymmetric patterns of connectivity, or with slow, local negative feedback, can generate sequential activity. This mechanism could account for preplay if the network only represented a single spatial map, or chart. However, global remapping in the hippocampus implies that multiple charts are represented simultaneously in the hippocampal network and it remains unknown whether the network with multiple charts can account for preplay. Here we show that it can. Driven with random inputs, the model generates sequences in every chart. Place fields in a given chart and OSA generated by the network are highly correlated. We also find significant correlations, albeit less frequently, even when the OSA is correlated with a new chart in which place fields are randomly scattered. These correlations arise from random correlations between the orderings of place fields in the new chart and those in a pre-existing chart. Our results suggest two different accounts for preplay. Either an existing chart is re-used to represent a novel environment or a new chart is formed.

While grid cells in the medial entorhinal cortex (MEC) of rodents have multiple, regularly arranged firing fields, place cells in the cornu ammonis (CA) regions of the hippocampus mostly have single spatial firing fields. Since there are extensive projections from MEC to the CA regions, many models have suggested that a feedforward network can transform grid cell firing into robust place cell firing. However, these models generate place fields that are consistently too small compared to those recorded in experiments. Here, we argue that it is implausible that grid cell activity alone can be transformed into place cells with robust place fields of realistic size in a feedforward network. We propose two solutions to this problem. Firstly, weakly spatially modulated cells, which are abundant throughout EC, provide input to downstream place cells along with grid cells. This simple model reproduces many place cell characteristics as well as results from lesion studies. Secondly, the recurrent connections between place cells in the CA3 network generate robust and realistic place fields. Both mechanisms could work in parallel in the hippocampal formation and this redundancy might account for the robustness of place cell responses to a range of disruptions of the hippocampal circuitry.

No abstract

Discriminating between object categories (e.g., conspecifics, food, potential predators) is a critical function of the primate and bird visual systems. We examined whether a similar hierarchical organization in the ventral stream that operates for processing faces in monkeys also exists in the avian visual system. We performed electrophysiological recordings from the pigeon Wulst of the thalamofugal pathway, in addition to the entopallium (ENTO) and mesopallium ventrolaterale (MVL) of the tectofugal pathway, while pigeons viewed images of faces, scrambled controls, and sine gratings. A greater proportion of MVL neurons fired to the stimuli, and linear discriminant analysis revealed that the population response of MVL neurons distinguished between the stimuli with greater capacity than ENTO and Wulst neurons. While MVL neurons displayed the greatest response selectivity, in contrast to the primate system no neurons were strongly face-selective and some responded best to the scrambled images. These findings suggest that MVL is primarily involved in processing the local features of images, much like the early visual cortex.