Neuronal Activity of the Young Hippocampus What Are Place Cells

Because single-cell recordings can be done while an animal is exploring an environment, the technique provides researchers with a view of the neurons of the hippocampus in action as it is processing spatial information in the rat (O'Keefe and Dostrovsky, 1971), the monkey (Rolls, 1999), and the human (Ekstrom et al., 2003). The best-researched of these is the freely moving rat. The pyramidal cells of the CA1 and CA3 hippocampus fire action potentials when the rat occupies particular places (for review, see Muller, 1996). ''Place cells'' have high firing rates in a particular area of an environment, referred to as the place field; outside this place field the cells are nearly silent (see examples of Figure 37.2).

In typical place cell experiments, the rat is placed into an environment, either an open field or a linear track. The rat then explores the arena, often with the encouragement of randomly placed food rewards. In the top row of the example (Figure 37.2) the rat is shown exploring cylindrical and square environments, which contain three distinct landmarks on the walls that the rat

Figure 37.2 Place fields of hippocampal cells in young and aged rats. The top row depicts the experimental setup with the rats exploring a familiar cylindrical arena (Cyl) and a novel square arena (Sq). Each subsequent row represents the activity of one cell over the entire experiment. Firing rate scales are provided on the left of the figure, such that darker pixels indicate areas in which more action potentials occurred. Sample tetrode waveforms of each cell are shown on the right side. Data are shown (a) for two place cells of two young rats and (b) for two cells of two aged, memory-impaired rats. Cell Y1 is an example of the generation of new spatial representations by cells of young rats. Cell Y2 shows a place cell whose field rotated, following the landmarks in the square. Cell A1 shows an example of rigid place fields of aged memory-impaired rats despite changes in the environment. Cell A2 is rigid in response to the first exposure to the novel-square, but then rotates with the square's landmarks in the second trial (Figure adapted from Wilson et al., 2003).

Figure 37.2 Place fields of hippocampal cells in young and aged rats. The top row depicts the experimental setup with the rats exploring a familiar cylindrical arena (Cyl) and a novel square arena (Sq). Each subsequent row represents the activity of one cell over the entire experiment. Firing rate scales are provided on the left of the figure, such that darker pixels indicate areas in which more action potentials occurred. Sample tetrode waveforms of each cell are shown on the right side. Data are shown (a) for two place cells of two young rats and (b) for two cells of two aged, memory-impaired rats. Cell Y1 is an example of the generation of new spatial representations by cells of young rats. Cell Y2 shows a place cell whose field rotated, following the landmarks in the square. Cell A1 shows an example of rigid place fields of aged memory-impaired rats despite changes in the environment. Cell A2 is rigid in response to the first exposure to the novel-square, but then rotates with the square's landmarks in the second trial (Figure adapted from Wilson et al., 2003).

can use for orientation. As the rat explores, the action potentials of pyramidal cells from the hippocampus are recorded. Each row in the figure depicts the activity of one neuron throughout the manipulations of the experiment. Each grid represents the floor space where the rat was moving. Dark pixels show high firing rates for a particular cell, whereas white pixels indicate no action potentials but that the rat did visit the area. The dark areas are referred to as the place field for that cell. Each time the rat passes through the place field, the place cell fires action potentials; outside the field the place cell is silent.

With thousands of cells active within an environment and each cell with its own place field, these neurons could compute the rat's spatial location and reflect elements of a rat's ''cognitive map'' (O'Keefe and Nadel, 1978). Wilson and McNaughton (1993), recording simultaneously from as many as 141 pyramidal cells, were able to estimate the rat's position to 1-cm accuracy even with only this number of cells. It is clear that these cells participate in a broad system of spatial processing that is important for navigation (Redish and Touretzky, 1997). The cells may also participate in a broader spectrum of memories; alternatives to the cognitive map theory posit that these cells could represent places where significant events occur within episodic memories (Eichenbaum et al., 1999) or participate in associations of contexts within memories (O'Reilly and Rudy, 2001; Redish, 2001).

Regardless of what they imply for hippocampal theory, place cells possess four characteristics that make them a useful window into how the hippocampus stores information, especially spatial information. The first property of place cells that attracts memory researchers is that they are not simply sensory neurons. The hippocampus receives multimodal information, so it is not a surprise that place fields are controlled by contributions from all the sensory modalities. Rats navigate by vision, smell, touch, hearing, and self-motion information; all of these have influence over place cell firing patterns (Muller, 1996). This characteristic means that researchers can study how the sensory modalities interact to control stored patterns of activity.

The second property of place cells that makes them attractive as a model of memory is their remarkable stability across time. Place cells are active in the same location with respect to each other and to the environment both within a continuous session in an environment and when the rat reenters the same environment after an absence (Muller and Kubie, 1987; Thompson and Best, 1990). This is clearly illustrated in cell Y1 in Figure 37.2. The cell is silent in the cylinder 1 environment. The rat is then removed from the arena and placed in a holding bucket while the arena is changed to a square out of the rat's sight. The rat is lifted back to the arena, and this process is repeated several times. Each of the three times that the rat explored the cylinder, this cell fired very few action potentials. The two exposures to the square arena, though, had distinct place fields in the same location; hence, the place fields were stable. This appears to be a function of memory recall because different environments are represented by different sets of place cells (discussed later), and reentering the original environment primes the retrieval of the original spatial representation. This characteristic of place cells indicates that a representation of the environment is stored in the hippocampus, and place cells allow researchers easy access to explore the mechanisms of these memories.

The third important feature of place cells is that they are largely controlled by visual landmarks, and therefore the place cells rotate with rotations of the visual landmarks. When the rat is removed from an arena and the visual landmarks of an arena are then rotated by 90°, upon reentry the place cells follow the landmark rotation by almost exactly 90° (Muller and Kubie, 1987; O'Keefe and Conway, 1978). This effect is shown in the cell Y2 of Figure 37.2. The place fields in the square environment have simply followed the 90° rotation of the landmarks (in this experiment the landmarks were the same in both environments, but rotated by 90°). Because tests of spatial memory, such as the water maze, rely upon use of the visual landmarks, the fact that place cells rotate with visual cues strengthens the link between hippocampal cells and spatial navigation. The rotations provide a simple way to test how well the cues of a particular environment control the hippocampal spatial representations.

The fourth attraction of place cells for memory researchers is the creation of new spatial representations in new environments. When a rat enters a visually new arena from a familiar one, the place cells drastically alter their place field firing patterns, quickly forming completely new firing patterns in the relation of the cells to each other and to the visual landmarks (Frank et al., 2004; Hill, 1978; Wilson and McNaughton, 1993). For two environments, two different sets of hippocampal neurons are active. Cell Y1 of Figure 37.2 illustrates a cell that is silent in one environment (the cylinder) and active in the other (the square). Alternatively, the cell may use two different place field locations to represent two environments. Each environment recalls into activity the unique network of neurons bound to it, much resembling a stored memory. The learning of a new environment and the creation of new spatial representation are not always rapid. When two environments are similar, place cells may initially use the same representation but with additional exposure may slowly (over as many as twenty days) develop distinct representations for each (Lever et al., 2002). Place cells, therefore, provide researchers the perfect opportunity to study the storage of a memory from its creation in the hippocampus.

In support of these assertions, several experiments have found that successful spatial navigation to a goal requires place fields consistent with that goal (Lenck-Santini et al., 2001; Lenck-Santini et al., 2002; O'Keefe and Speakman, 1987; Rosenzweig et al., 2003). For example, in a study by Lenck-Santini and colleagues (2001) rats performed a continuous spatial alternation task in a 3-armed Y-maze. After a series of landmark rotations, some place fields became out-of-register with the goal arm, and for these rats, performance on the task was poor. Place fields of other rats maintained their correct relationship with the goal arm, and for these rats, performance on the task remained accurate. These studies strongly suggest that a consistent place field-goal relationship is essential for finding goals that require spatial navigation.

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