Firing patterns of hippocampal complex-spike neurons were examined for the capacity to encode information important to the memory demands of a task even when the overt behavior and location of the animal are held constant. Neuronal activity was recorded as rats continuously alternated left and right turns from the central stem of a modified T maze. Two-thirds of the cells fired differentially as the rat traversed the common stem on left-turn and right-turn trials, even when potentially confounding variations in running speed, heading, and position on the stem were taken into account. Other cells fired differentially on the two trial types in combination with behavioral and spatial factors or appeared to fire similarly on both trial types. This pattern of results suggests that hippocampal representations encode some of the information necessary for representing specific memory episodes.
In humans the hippocampal region of the brain is crucial for declarative or episodic memory for a broad range of materials. In contrast, there has been controversy over whether the hippocampus mediates a similarly general memory function in other species, or whether it is dedicated to spatial memory processing. Evidence for the spatial view is derived principally from the observations of 'place cells'-hippocampal neurons that fire whenever the animal is in a particular location in its environment, or when it perceives a specific stimulus or performs a specific behaviour in a particular place. We trained rats to perform the same recognition memory task in several distinct locations in a rich spatial environment and found that the activity of many hippocampal neurons was related consistently to perceptual, behavioural or cognitive events, regardless of the location where these events occurred. These results indicate that nonspatial events are fundamental elements of hippocampal representation, and support the view that, across species, the hippocampus has a broad role in information processing associated with memory.
and more recently in animals as well (Eichenbaum, 1997). Furthermore, several recent electrophysiological McGill University Montreal PQH3A 1B1 studies have revealed properties of hippocampal neuronal firing patterns that are inconsistent with the notion Canada ‡ Department of Neuroscience and Neurology of a cognitive map and indicate a broader scope of information processing. This paper will focus on these University and University Hospital of Kuopio 70211 Kuopio studies, reviewing some of the history and basic properties of place cells, and considering both early and recent Finland findings that shed light on the content and organization of information encoded within hippocampal neuronal activity. We will call into question the cognitive map Identifying the scope and nature of memory processing by the hippocampus has proved a formidable challenge. account and offer an alternative view. The major initial insights came from studies of amnesia in human patients following removal of the hippocampus Why Place Cells Are So Compelling: Pointers plus neighboring medial temporal structures (Scoville in the Cognitive Map and Milner, 1957). The early studies indicated that this In the early years of investigations on animal learning, damage spares the initial acquisition of new information, proponents of the dominant "stimulus-response" ("S-R") but memory for all sorts of new information subsetheory argued that maze learning is mediated by a chain quently declines rapidly. More recent studies have of direct associations between specific stimuli and reshown that global amnesia results from limited damage warded behavioral responses. However, Edward Tolwithin the hippocampus itself (Zola-Morgan et al., 1986) man (1948) provided compelling evidence that rats can or including the hippocampus and dentate gyrus and navigate mazes using short cuts and roundabout routes sparing most or all of the surrounding cortex and other to find goal locations, strategies that were not readily medial temporal structures (Vargha-Khadem et al., explained by S-R theory. Tolman concluded that rats 1997). These findings indicate that the hippocampus create and use global representations of the environplays a critical role in memory formation for a broad ment, that is, cognitive maps, to localize goals in a maze. domain of information in humans. This view was criticized for the absence of evidence for Many studies have sought to clarify the nature of hipa cognitive or neural mechanism that could underlie the pocampal information processing, using neuropsychocognitive map-something as compelling as the physiological and electrophysiological approaches in animals. logical observations on the conditioned reflexes that Among several proposals generated by these studies, were viewed to mediate S-R learning. In the initial report one that has captured considerable attention is the view on the discovery of place cells, O'Keefe and Dostrovsky that the hippocampus mediates a neural representation (1971) recognized the potential significance of this neuof phy...
Previous research has shown that head direction (HD) cells in both the anterior dorsal thalamus (ADN) and the postsubiculum (PoS) in rats discharge in relation to familiar, visual landmarks in the environment. This study assessed whether PoS and ADN HD cells would be similarly responsive to nonvisual or unfamiliar environmental cues. After visual input was eliminated by blindfolding the rats, HD cells maintained direction-specific discharge, but their preferred firing directions became less stable. In addition, rotations of the behavioral apparatus indicated that some nonvisual cues (presumably tactile, olfactory, or both) exerted above chance stimulus control over a cell's preferred firing direction. However, a prominent auditory cue was not effective in exerting stimulus control over a cell's preferred direction. HD cell activity also was assessed after rotation of a novel visual cue exposed to the rat for 1, 3, or 8 min. An 8-min exposure was enough time for a novel visual cue to gain control over a cell's preferred direction, whereas an exposure of 1 or 3 min led to control in only about half the sessions. These latter results indicate that HD cells rely on a rapid learning mechanism to develop associations with landmark cues. Previous studies have identified neurons in the postsubiculum (PoS) and anterior dorsal nucleus of the thalamus (ADN) of the rat that discharge as a function of the animal's head direction (HD) in the horizontal plane (Taube, 1995; Taube, Mullei, & Ranck, 1990a). HD cells are maximally active when the rat is pointing its head in one particular direction (the "preferred direction"), and their firing rate declines gradually as its head turns away from this direction. In addition to the PoS and ADN, HD cells have been identified in the lateral dorsal thalamus (LDN; Mizumori & Williams, 1993), striatum (Wiener, 1993), lateral mammillary nuclei (Stackman & Taube, 1998), and retrosplenial cortex (Chen et al., 1994). Research also has shown that PoS and ADN HD cells are responsive to the position of familiar visual landmarks (Taube, 1995; Taube, Muller, & Ranck, 1990b). For example, when a familiar visual cue is rotated, the cell's preferred direction usually shifts by a corresponding amount. The current study was designed to explore two issues concerning external landmark control over HD cell discharge. First, we examined the role of nonvisual, environmental cues (e.g., tactile, olfactory, or auditory) in influencing
Recent work has shown that lesions of the hippocampus in monkeys cause deficits in the capacity to remember increasing numbers of objects, colors, and spatial locations (). However, others have observed that hippocampectomized monkeys can show intact memory for a list of objects or locations (). We wished to explore the effects of hippocampal damage on the capacity of memory in the rodent and, to do so, developed novel "span" tasks in which a variable number of odors or locations had to be remembered. In the odor span task (experiment 1), rats were trained on a nonmatching to sample task in which increasing numbers of odors had to be remembered. Half of the trained rats received ibotenic acid lesions of the hippocampus. Postoperatively, hippocampectomized animals did not differ from control animals even when required to remember up to 24 odors. However, when tested on delayed retention of a list of 12 odors, rats with hippocampal lesions were impaired at a long delay. Also, these rats were impaired on a subsequent test of delayed spatial alternation. In a spatial span task (experiment 2), naive rats were trained on a nonmatching to sample task in which a variable number of locations had to be remembered. After this, half of the animals received ibotenic acid lesions. Postoperatively, hippocampectomized animals performed above chance levels when required to remember a single cup location, but were unable to remember more. Subsequent testing on another spatial delayed alternation task suggested that hippocampectomized rats could recognize, but could not inhibit their approach to previously visited locations.
The occurrence of cells that encode spatial location (place cells) or head direction (HD cells) in the rat limbic system suggests that these cell types are important for spatial navigation. We sought to determine whether place fields of hippocampal CA1 place cells would be altered in animals receiving lesions of brain areas containing HD cells. Rats received bilateral lesions of anterodorsal thalamic nuclei (ADN), postsubiculum (PoS), or sham lesions, before place cell recording. Although place cells from lesioned animals did not differ from controls on many place-field characteristics, such as place-field size and infield firing rate, the signal was significantly degraded with respect to measures of outfield firing rate, spatial coherence, and information content. Surprisingly, place cells from lesioned animals were more likely modulated by the directional heading of the animal. Rotation of the landmark cue showed that place fields from PoS-lesioned animals were not controlled by the cue and shifted unpredictably between sessions. Although fields from ADN-lesioned animals tended to have less landmark control than fields from control animals, this impairment was mild compared with cells recorded from PoS-lesioned animals. Removal of the prominent visual cue also led to instability of place-field representations in PoS-lesioned, but not ADN-lesioned, animals. Together, these findings suggest that an intact HD system is not necessary for the maintenance of place fields, but lesions of brain areas that convey the HD signal can degrade this signal, and lesions of the PoS might lead to perceptual or mnemonic deficits, leading to place-field instability between sessions.
There is a growing body of evidence that important aspects of human cognition have been marginalized, or overlooked, by traditional cognitive science. In particular, the use of laboratory-based experiments in which stimuli are artificial, and response options are fixed, inevitably results in findings that are less ecologically valid in relation to real-world behavior. In the present review we highlight the opportunities provided by a range of new mobile technologies that allow traditionally lab-bound measurements to now be collected during natural interactions with the world. We begin by outlining the theoretical support that mobile approaches receive from the development of embodied accounts of cognition, and we review the widening evidence that illustrates the importance of examining cognitive processes in their context. As we acknowledge, in practice, the development of mobile approaches brings with it fresh challenges, and will undoubtedly require innovation in paradigm design and analysis. If successful, however, the mobile cognition approach will offer novel insights in a range of areas, including understanding the cognitive processes underlying navigation through space and the role of attention during natural behavior. We argue that the development of real-world mobile cognition offers both increased ecological validity, and the opportunity to examine the interactions between perception, cognition and action—rather than examining each in isolation.
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