Brain aging: impaired coding of novel environmental cues - PubMed (original) (raw)

Brain aging: impaired coding of novel environmental cues

H Tanila et al. J Neurosci. 1997.

Abstract

Studies of the spatial memory capacities of aged animals usually focus on performance during the learning of new environments. By contrast, efforts to characterize age-related alterations in spatial firing information processing by hippocampal neurons typically use an environment that is highly familiar to the animals. In the present study we compared the firing properties of hippocampal neurons in young adult and aged rats as they acquired spatial information about new environmental cues. Hippocampal complex spike cells were recorded while rats performed a radial arm maze task in a familiar environment and then recorded again after many of the spatial cues were changed. After the change in the environment, in aged rats 35-42% of place fields retained their original shape and location with respect to the maze center, although they usually rotated to another arm. By contrast, all place fields in young animals either disappeared or appeared in a new location. Some of the new place fields appeared in the new environment during the first 5 min of exploration, whereas others needed more than 30 min to develop fully. In the familiar environment spatial selectivity of place cells was similar in young and aged rats. By contrast, when rats were placed into a new environment, spatial selectivity decreased considerably in aged memory-impaired rats compared with that of young rats and aged rats with intact memory performance.

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Figures

Fig. 1.

Fig. 1.

Schematic illustration of the recording environments. In the familiar environment the maze was screened from the rest of room by black curtains (185 cm wide) extending from the floor to 30 cm from the ceiling (curtains are white for clarity). On the four walls of the curtain were hanging clearly distinguishable landmark cards. The maze was covered with insertable surfaces differing in texture and smell. In new environment 1 (NEW 1) a colorful pillowcase was a prominent landmark in one corner (top right corner). The curtains were drawn from two walls, revealing a view to the experimenter with a computer and an instrument rack. In new environment 2 (NEW 2) only blank white laboratory walls were visible through the openings in the curtained enclosure. A white and green plastic bag hanging from the ceiling was the only prominent landmark. The mazes were covered with odorless wooden black surfaces in both new environments.

Fig. 2.

Fig. 2.

Raw firing rate maps recorded from an aged memory-intact rat. A, Distribution of firing rates in the familiar environment. B, Firing rate maps in the new environment for the first, second, and fourth 5 min trials. The place field rotates 180° with the change of the environment. Spatial selectivities are: familiar environment, 20.7; and new environment after 5 min, 9.4; after 10 min, 16.6; and after 20 min, 16.4. Note that the gratings are relative, so that the pixel with the highest firing rate in each icon is black. The corresponding firing rates are shown by the numbers to the_right_ of each icon. C, Waveform of the neuron recorded with a tetrode. Each curve represents superimposed waveforms recorded from each one of the four tips of the electrode.

Fig. 3.

Fig. 3.

Raw firing rate maps recorded from an aged memory-impaired rat. A, Familiar environment.B, First, second, fourth, and fifth 5 min trials in the new environment. C, Return to the familiar environment.D, Waveform of the neuron recorded with a tetrode. After exposure to the new environment the shape of the place field slightly changes, but the location remains in the same position with respect to the maze and the room. After the 30 min exploration of the new environment, the place field unexpectedly rotates 90° counterclockwise (50 min). After return of the rat to the familiar environment the place field appeared rotated 90° clockwise compared with its original orientation.

Fig. 4.

Fig. 4.

Raw firing rate maps recorded from a young rat. The neuron does not fire at all in the familiar environment (A), but a clear place field appears during the first 5 min trial in the new environment. Spatial selectivity of the place field increased during the following 15 min exposure to the new environment, however (spatial selectivities: 5 min, 134.3; 10 min, 345.2; and 20 min, >500). Other explanations are as in Figure 2.

Fig. 5.

Fig. 5.

Raw firing rate maps and field maps from a recording of a young rat. The field maps are to the_right_ of the raw firing rate maps for the familiar environment (A, C) and_below_ the raw firing rate maps for the new environment (B). Initially there is brisk activity, and the firing is focused on two locations (A). In the new environment the total activity radically decreases, and no place fields can be determined during the first 20 min exposure. After the 30 min free exploration of the new environment, a new place field can be seen (B, 50 min). After the rat was returned to the familiar environment, the total activity of the neuron was considerably reduced compared with the first trial, but the same spatial distribution of firing could still be observed (C). D, Waveform of the neuron as recorded with four tips of the tetrode.

Fig. 6.

Fig. 6.

Mean spatial selectivity of all neurons in the three experimental groups. The spatial selectivity decreased in all groups during the first 5 min trial in the new environment (NEW 1). In young and aged memory-intact rats the spatial selectivity increased above the initial level within 20 min of exposure to the new environment. In the aged memory-impaired rats spatial selectivity in the new environment remained low until they were given a 30 min free exploration time (between NEW 4 and_NEW 5_). Note the drop of spatial selectivity in young and aged intact animals after return to the familiar environment (FAM 2), which is in contrast with the further increase in spatial selectivity in aged memory-impaired rats.

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