Key Features of Human Episodic Recollection in the Cross-Episode Retrieval of Rat Hippocampus Representations of Space

Neurophysiological studies focus on memory retrieval as a reproduction of what was experienced and have established that neural discharge is replayed to express memory. However, cognitive psychology has established that recollection is not a verbatim replay of stored information. Recollection is constructive, the product of memory retrieval cues, the information stored in memory, and the subject''s state of mind. We discovered key features of constructive recollection embedded in the rat CA1 ensemble discharge during an active avoidance task. Rats learned two task variants, one with the arena stable, the other with it rotating; each variant defined a distinct behavioral episode. During the rotating episode, the ensemble discharge of CA1 principal neurons was dynamically organized to concurrently represent space in two distinct codes. The code for spatial reference frame switched rapidly between representing the rat''s current location in either the stationary spatial frame of the room or the rotating frame of the arena. The code for task variant switched less frequently between a representation of the current rotating episode and the stable episode from the rat''s past. The characteristics and interplay of these two hippocampal codes revealed three key properties of constructive recollection. (1) Although the ensemble representations of the stable and rotating episodes were distinct, ensemble discharge during rotation occasionally resembled the stable condition, demonstrating cross-episode retrieval of the representation of the remote, stable episode. (2) This cross-episode retrieval at the level of the code for task variant was more likely when the rotating arena was about to match its orientation in the stable episode. (3) The likelihood of cross-episode retrieval was influenced by preretrieval information that was signaled at the level of the code for spatial reference frame. Thus key features of episodic recollection manifest in rat hippocampal representations of space.     

Hippocampal "time cells" bridge the gap in memory for discontiguous events

The hippocampus is critical to remembering the flow of events in distinct experiences and, in doing so, bridges temporal gaps between discontiguous events. Here, we report a robust hippocampal representation of sequence memories, highlighted by "time cells" that encode successive moments during an empty temporal gap between the key events, while also encoding location and ongoing behavior. Furthermore, just as most place cells "remap" when a salient spatial cue is altered, most time cells form qualitatively different representations ("retime") when the main temporal parameter is altered. Hippocampal neurons also differentially encode the key events and disambiguate different event sequences to compose unique, temporally organized representations of specific experiences. These findings suggest that hippocampal neural ensembles segment temporally organized memories much the same as they represent locations of important events in spatially defined environments.     

New experiences enhance coordinated neural activity in the hippocampus

The acquisition of new memories for places and events requires synaptic plasticity in the hippocampus, and plasticity depends on temporal coordination among neurons. Spatial activity in the hippocampus is relatively disorganized during the initial exploration of a novel environment, however, and it is unclear how neural activity during the initial stages of learning drives synaptic plasticity. Here we show that pairs of CA1 cells that represent overlapping novel locations are initially more coactive and more precisely coordinated than are cells representing overlapping familiar locations. This increased coordination occurs specifically during brief, high-frequency events (HFEs) in the local field potential that are similar to ripples and is not associated with better coordination of place-specific neural activity outside of HFEs. As novel locations become more familiar, correlations between cell pairs decrease. Thus, hippocampal neural activity during learning has a unique structure that is well suited to induce synaptic plasticity and to allow for rapid storage of new memories.     

大脑前额叶是怎样处理空间信息的

我们的大脑可能使用多个参考系来处理空间信息,比如使用"自我为中心的参考系"和"以大环境为参考系"来处理空间信息。灵长类大脑前额叶位于大脑皮层额叶的前端,尽管对前额叶在脑高级功能中的作用谁都不会怀疑,但很多具体的细节还是不甚清楚,比如背侧大脑前额叶在处理工作记忆信息时,是否处理所有的空间工作记忆信息?该文首先回顾对前额叶的研究情况,然后讨论背侧前额叶在处理自我为中心的空间信息中的作用,最后指出背侧前额叶仅对自我为中心的空间信息处理负责,而与大环境为中心的空间信息处理无关。     

A neural mechanism for coordinate transformation predicts pre-saccadic remapping

Whenever we shift our gaze, any location information encoded in the retinocentric reference frame that is predominant in the visual system is obliterated. How is spatial memory retained across gaze changes? Two different explanations have been proposed: Retinocentric information may be transformed into a gaze-invariant representation through a mechanism consistent with gain fields observed in parietal cortex, or retinocentric information may be updated in anticipation of the shift expected with every gaze change, a proposal consistent with neural observations in LIP. The explanations were considered incompatible with each other, because retinocentric update is observed before the gaze shift has terminated. Here, we show that a neural dynamic mechanism for coordinate transformation can also account for retinocentric updating. Our model postulates an extended mechanism of reference frame transformation that is based on bidirectional mapping between a retinocentric and a body-centered representation and that enables transforming multiple object locations in parallel. The dynamic coupling between the two reference frames generates a shift of the retinocentric representation for every gaze change. We account for the predictive nature of the observed remapping activity by using the same kind of neural mechanism to generate an internal representation of gaze direction that is predictively updated based on corollary discharge signals. We provide evidence for the model by accounting for a series of behavioral and neural experimental observations.     

Rhythmic modulation of theta oscillations supports encoding of spatial and behavioral information in the rat hippocampus

Oscillatory patterns of activity in various frequency ranges are ubiquitously expressed in cortical circuits. While recent studies in humans emphasized rhythmic modulations of neuronal oscillations ("second-order" rhythms), their potential involvement in information coding remains an open question. Here, we show that a rhythmic (～0.7?Hz) modulation of hippocampal theta power, unraveled by second-order spectral analysis, supports encoding of spatial and behavioral information. The phase preference of neuronal discharge within this slow rhythm significantly increases the amount of information carried by action potentials in various motor/cognitive behaviors by (1) distinguishing between the spikes fired within versus outside the place field of hippocampal place cells, (2) disambiguating place firing of neurons having multiple place fields, and (3) predicting between alternative future spatial trajectories. This finding demonstrates the relevance of second-order spectral components of brain rhythms for decoding neuronal information.     

Dissociation of exteroceptive and idiothetic orientation cues: effect on hippocampal place cells and place navigation.

Navigation by means of cognitive maps appears to require the hippocampus; hippocampal place cells (PCs) appear to store spatial memories because their discharge is confined to cell-specific places called firing fields (FFs). Experiments with rats manipulated idiothetic and landmark-related information to understand the relationship between PC activity and spatial cognition. Rotating a circular arena in the light caused a discrepancy between these cues. This discrepancy caused most FFs to disappear in both the arena and room reference frames. However, FFs persisted in the rotating arena frame when the discrepancy was reduced by darkness or by a card in the arena. The discrepancy was increased by ''field clamping'' the rat in a room-defined FF location by rotations that countered its locomotion. Most FFs dissipated and reappeared an hour or more after the clamp. Place-avoidance experiments showed that navigation uses independent idiothetic and exteroceptive memories. Rats learned to avoid the unmarked footshock region within a circular arena. When acquired on the stable arena in the light, the location of the punishment was learned by using both room and idiothetic cues; extinction in the dark transferred to the following session in the light. If, however, extinction occurred during rotation, only the arena-frame avoidance was extinguished in darkness; the room-defined location was avoided when the lights were turned back on. Idiothetic memory of room-defined avoidance was not formed during rotation in light; regardless of rotation, there was no avoidance when the lights were turned off, but room-frame avoidance reappeared when the lights were turned back on. The place-preference task rewarded visits to an allocentric target location with a randomly dispersed pellet. The resulting behaviour alternated between random pellet searching and target-directed navigation, making it possible to examine PC correlates of these two classes of spatial behaviour. The independence of idiothetic and exteroceptive spatial memories and the disruption of PC firing during rotation suggest that PCs may not be necessary for spatial cognition; this idea can be tested by recordings during the place-avoidance and preference tasks.     

Multimodal integration for the representation of space in the posterior parietal cortex.

The posterior parietal cortex has long been considered an ''association'' area that combines information from different sensory modalities to form a cognitive representation of space. However, until recently little has been known about the neural mechanisms responsible for this important cognitive process. Recent experiments from the author''s laboratory indicate that visual, somatosensory, auditory and vestibular signals are combined in areas LIP and 7a of the posterior parietal cortex. The integration of these signals can represent the locations of stimuli with respect to the observer and within the environment. Area MSTd combines visual motion signals, similar to those generated during an observer''s movement through the environment, with eye-movement and vestibular signals. This integration appears to play a role in specifying the path on which the observer is moving. All three cortical areas combine different modalities into common spatial frames by using a gain-field mechanism. The spatial representations in areas LIP and 7a appear to be important for specifying the locations of targets for actions such as eye movements or reaching; the spatial representation within area MSTd appears to be important for navigation and the perceptual stability of motion signals.     

The mechanism of rate remapping in the dentate gyrus

Rate remapping is a recently revealed neural code in which sensory information modulates the firing rate of hippocampal place cells. The mechanism underlying rate remapping is unknown. Its characteristic modulation, however, must arise from the interaction of the two major inputs to the hippocampus, the medial entorhinal cortex (MEC), in which grid cells represent the spatial position of the rat, and the lateral entorhinal cortex (LEC), in which cells represent the sensory properties of the environment. We have used computational methods to elucidate the mechanism by which this interaction produces rate remapping. We show that the convergence of LEC and MEC inputs, in conjunction with a competitive network process mediated by feedback inhibition, can account quantitatively for this phenomenon. The same principle accounts for why different place fields of the same cell vary independently as sensory information is altered. Our results show that rate remapping can be explained in terms of known mechanisms.     

Place cells, spatial maps and the population code for memory

The study of population dynamics in hippocampal place cells has emerged as one of the most powerful tools for understanding the encoding, storage and retrieval of declarative memory. Recent work has laid out the contours of an attractor-based hippocampal population code for memory in recurrent circuits of the hippocampus. The code is based on inputs from a topographically organized, path-integration-dependent spatial map that lies upstream in the medial entorhinal cortex. The recurrent networks of the hippocampal formation enable these spatial inputs to be synthesized with nonspatial event-related information.     

Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations,movement between goals,and environmental context in a radial-arm arena

The amniote hippocampal formation plays an evolutionarily-conserved role in the neural representation of environmental space. However, species differences in spatial ecology nurture the expectation of species differences in how hippocampal neurons represent space. To determine the spatial response properties of homing pigeon (Columba livia) HFneurons, we recorded from isolated units in birds freely navigating a radial arena in search of food present at four goal locations. Fifty of 76 neurons displayed firing rate variations that could be placed into three response categories. Location cells (n=25) displayed higher firing rates at restricted locations in the arena space, often in proximity to goal locations. Path cells (n=13) displayed higher firing rates as a pigeon moved between a subset of goal locations. Arena-off cells (n=12) were more active when a pigeon was in a baseline holding space compared to inside the arena. Overall, reliability and coherence scores of the recorded neurons were lower compared to rat place cells. The differences in the spatial response profiles of pigeon hippocampal formation neurons, when compared to rats, provide a departure point for better understanding the relationship between spatial behavior and how hippocampal formation neurons participate in the representation of space.     

Responses of brainstem lateral line units to different stimulus source locations and vibration directions

We recorded responses of lateral line units in the medial octavolateralis nucleus in the brainstem of goldfish, Carassius auratus, to a 50 Hz vibrating sphere and studied how responses were affected by placing the sphere at various locations alongside the fish and by different directions of vibration. In most units (88%), stimulation with the sphere from one or more spatial locations caused an increase and/or decrease in discharge rate. In few units (10%), discharge rate was increased by stimulation from one location and decreased by stimulation from an adjacent location in space. In a minority of the units (2%), changing sphere location did not affect discharge rates but caused a change in phase coupling. Units sensitive to a distinct sphere vibration direction were not found. The data also show that the responses of most brainstem units differ from those of primary afferent nerve fibers. Whereas primary afferents represent the pressure gradient pattern generated by the sphere and thus encode location and vibration direction of a vibrating sphere, most brainstem units do not. This information may be represented in the brainstem by a population code or in higher centers of the ascending lateral line pathway.     

A common reference frame for movement plans in the posterior parietal cortex

Orchestrating a movement towards a sensory target requires many computational processes, including a transformation between reference frames. This transformation is important because the reference frames in which sensory stimuli are encoded often differ from those of motor effectors. The posterior parietal cortex has an important role in these transformations. Recent work indicates that a significant proportion of parietal neurons in two cortical areas transforms the sensory signals that are used to guide movements into a common reference frame. This common reference frame is an eye-centred representation that is modulated by eye-, head-, body- or limb-position signals. A common reference frame might facilitate communication between different areas that are involved in coordinating the movements of different effectors. It might also be an efficient way to represent the locations of different sensory targets in the world.     

Attention Enhances the Retrieval and Stability of Visuospatial and Olfactory Representations in the Dorsal Hippocampus

A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippocampus while mice acquired one of two goal-oriented tasks. These tasks required the animals to find a hidden food reward by attending to either the visuospatial environment or a particular odor presented in shifting spatial locations. Attention to the visuospatial environment increased the stability of visuospatial representations and phase locking to gamma oscillations—a form of neuronal synchronization thought to underlie the attentional mechanism necessary for processing task-relevant information. Attention to a spatially shifting olfactory cue compromised the stability of place fields and increased the stability of reward-associated odor representations, which were most consistently retrieved during periods of sniffing and digging when animals were restricted to the cup locations. Together, these results suggest that attention selectively modulates the encoding and retrieval of hippocampal representations by enhancing physiological responses to task-relevant information.     

Temporal encoding of place sequences by hippocampal cell assemblies

Both episodic memory and spatial navigation require temporal encoding of the relationships between events or locations. In a linear maze, ordered spatial distances between sequential locations were represented by the temporal relations of hippocampal place cell pairs within cycles of theta oscillation in a compressed manner. Such correlations could arise due to spike "phase precession" of independent neurons driven by common theta pacemaker or as a result of temporal coordination among specific hippocampal cell assemblies. We found that temporal correlation between place cell pairs was stronger than predicted by a pacemaker drive of independent neurons, indicating a critical role for synaptic interactions and precise timing within and across cell assemblies in place sequence representation. CA1 and CA3 ensembles, identifying spatial locations, were active preferentially on opposite phases of theta cycles. These observations suggest that interleaving CA3 neuronal sequences bind CA1 assemblies representing overlapping past, present, and future locations into single episodes.     

Spatial learning and action planning in a prefrontal cortical network model

The interplay between hippocampus and prefrontal cortex (PFC) is fundamental to spatial cognition. Complementing hippocampal place coding, prefrontal representations provide more abstract and hierarchically organized memories suitable for decision making. We model a prefrontal network mediating distributed information processing for spatial learning and action planning. Specific connectivity and synaptic adaptation principles shape the recurrent dynamics of the network arranged in cortical minicolumns. We show how the PFC columnar organization is suitable for learning sparse topological-metrical representations from redundant hippocampal inputs. The recurrent nature of the network supports multilevel spatial processing, allowing structural features of the environment to be encoded. An activation diffusion mechanism spreads the neural activity through the column population leading to trajectory planning. The model provides a functional framework for interpreting the activity of PFC neurons recorded during navigation tasks. We illustrate the link from single unit activity to behavioral responses. The results suggest plausible neural mechanisms subserving the cognitive "insight" capability originally attributed to rodents by Tolman & Honzik. Our time course analysis of neural responses shows how the interaction between hippocampus and PFC can yield the encoding of manifold information pertinent to spatial planning, including prospective coding and distance-to-goal correlates.     

Rate remapping: when the code goes beyond space

Rate remapping is a conjunctive code that potentially enables hippocampal place cells to jointly represent spatial and nonspatial information. In this issue of Neuron, Rennó-Costa et al. introduce a theoretical model wherein the convergence of the medial and lateral entorhinal excitatory inputs, combined with local inhibition, explains hippocampal rate remapping.     

Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity

 A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learning is applied to map place cell activity into action cell activity. The ensemble action cell activity provides navigational maps to support spatial behavior. We present experimental results obtained with a mobile Khepera robot. Received: 02 July 1999 / Accepted in revised form: 20 March 2000     

Coding of the reach vector in parietal area 5d

Competing models of sensorimotor computation predict different topological constraints in the brain. Some models propose population coding of particular reference frames in anatomically distinct nodes, whereas others require no such dedicated subpopulations and instead predict that regions will simultaneously code in multiple, intermediate, reference frames. Current empirical evidence is conflicting, partly due to difficulties involved in identifying underlying reference frames. Here, we independently varied the locations of hand, gaze, and target over many positions while recording from the dorsal aspect of parietal area 5. We find that the target is?represented in a predominantly hand-centered reference frame here, contrasting with the relative code seen in dorsal premotor cortex and the mostly gaze-centered reference frame in the parietal reach region. This supports the hypothesis that different nodes of the sensorimotor circuit contain distinct and systematic representations, and this constrains the types of computational model that are neurobiologically relevant.     

The human hippocampus and spatial and episodic memory

Finding one's way around an environment and remembering the events that occur within it are crucial cognitive abilities that have been linked to the hippocampus and medial temporal lobes. Our review of neuropsychological, behavioral, and neuroimaging studies of human hippocampal involvement in spatial memory concentrates on three important concepts in this field: spatial frameworks, dimensionality, and orientation and self-motion. We also compare variation in hippocampal structure and function across and within species. We discuss how its spatial role relates to its accepted role in episodic memory. Five related studies use virtual reality to examine these two types of memory in ecologically valid situations. While processing of spatial scenes involves the parahippocampus, the right hippocampus appears particularly involved in memory for locations within an environment, with the left hippocampus more involved in context-dependent episodic or autobiographical memory.