Article Figures & Data
Figures
- Fig. 1.
The amplitude of extracellularly recorded spikes decreases as an animal runs through the place field of a cell.A, B, Amplitude of individual spikes, from two representative hippocampal pyramidal cells, plotted as a function of the rat's location on a track. The cells were directionally tuned and fired as the animal moved from left toright on the x-axis. The amplitude of each spike is expressed as a percentage of the maximum spike amplitude recorded from the cell. Insets, The waveforms of three spikes recorded from a single-tetrode channel. Because a systematic decrease in amplitude was seen simultaneously on all four channels of the tetrode, the spikes are assumed to have originated from the cell.Colored boxes outline those spikes whose waveforms are depicted in the insets. Amp, Amplitude;Max, maximum.
- Fig. 2.
Activity-dependent attenuation in spike amplitude is reduced with experience. A, The average (± SE) amplitude attenuation during high-frequency bursts for a population of simultaneously recorded cells. The amplitude of the last spike in a burst is expressed as a fraction of the amplitude of the first spike and is plotted as a function of the number of spikes in the burst. Theblack line plots the average attenuation for the animal's first 4 min in the environment, and the gray line plots the attenuation for the animal's last 4 min. Notice that the amount of attenuation is reduced with experience (anasterisk indicates a significant difference,p < 0.05, paired t test).B, The average attenuation for bursts of three spikes for both the first 4 min (black bars) and last 4 min (gray bars) of an animal's experience in a familiar environment. A significant (*p < 0.05, t test) reduction in amplitude attenuation was seen in seven of the seven data sets.
- Fig. 3.
Time course of changes in amplitude attenuation during behavior. Average (± SE) amplitude attenuation within bursts of three spikes as a function of the time spent within an environment.
- Fig. 4.
Experience-dependent reductions in amplitude attenuation are context specific.A, Two animals were allowed to run on one familiar track and then immediately transferred to a second familiar track. A subset of hippocampal cells (n = 48) was active on both tracks. For these cells, the average amplitude attenuation for bursts of three spikes is shown. The black bars show the average attenuation for the animal's first 4 min in the environment, and the gray bars show the average attenuation for the animal's last 4 min. Notice that in the first environment (track 1), bursts showed an experience-dependent reduction in amplitude attenuation (*p < 0.05, ttest). When the animal was transferred to the second environment (track 2), the amount of attenuation initially increased relative to that in the last 4 min in the first environment but was once again reduced with experience (*p < 0.05, ttest). B, To determine whether handling alone was sufficient to cause reductions in amplitude attenuation to reset when an animal was transferred from one track to another, one animal was returned to track 1 after experience on track 2. For this animal, a total of 21 hippocampal cells were active on both tracks. For these cells, the average amplitude attenuation for bursts of three spikes is shown. The black bars show the average attenuation for the animal's first 4 min in the environment, and the gray bars show the average attenuation for the animal's last 4 min. When the animal was returned to the first environment (track 1), the amount of attenuation was the same as when the animal left this environment, suggesting that handling alone does not cause the amount of attenuation to return to baseline.
- Fig. 5.
The effective connectivity between hippocampal pyramidal cells and interneurons is increased with an animal's experience in an environment. Normalized cross-correlation histograms were computed for pairs of pyramidal cells and interneurons recorded from the same tetrode during behavior (see Results). A, B, Normalized cross-correlation histograms for one pyramidal cell–interneuron pair for both the animal's first 4 min (A) and last 4 min (B) in an environment. The short-latency (2–3 msec) peak in the cross-correlation histogram represents a putative monosynaptic connection between the pyramidal cell and interneuron (dotted line at 3 SD above mean, p < 0.0013). For this cell pair, the magnitude of the monosynaptic peak increases with experience, suggesting an experience-dependent increase in effective coupling. For these experiments, 9 of 12 “coupled” pyramidal cell–interneuron pairs showed an experience-dependent increase in effective connectivity (p < 0.05, sign test).
- Fig. 6.
Pharmacological blockade of NMDA receptors impairs experience-dependent reductions in amplitude attenuation.A, For one recording session, the average (± SE) amplitude attenuation during high-frequency bursts. The amplitude of the last spike in a burst is expressed as a fraction of the amplitude of the first spike and is plotted as a function of the number of spikes in the burst. The black line plots the average attenuation for the animal's first 4 min in the environment, and thegray line plots the attenuation for the animal's last 4 min. Notice that there is no experience-dependent reduction in amplitude attenuation. B, The average attenuation for bursts of three spikes for both the first 4 min (black bars) and last 4 min (gray bars) of an animal's experience in a familiar environment. Only one of the eight data sets showed a significant (*p < 0.05,t test) reduction in amplitude attenuation.
- Fig. 7.
Extracellular electrodes record from a local volume of tissue, and as a consequence an extracellular action potential may reflect an integrated signal from both the soma and proximal dendrites of a hippocampal pyramidal cell. Top, During a burst of action potentials there is an activity-dependent decrease in the ability of later spikes within a burst to back-propagate actively into the cell's dendrites. This activity-dependent decrease in effective back-propagation may manifest as a decrease in the amplitude of extracellularly recorded spikes (A, extracellularly recorded signal; B, intracellular somatic signal; C, intracellular signal from proximal dendrites; D, intracellular signal from distal dendrites). Bottom, An experience-dependent reduction in the degree to which extracellularly recorded action potentials show activity-dependent attenuations in spike amplitude may reflect an increase in the effectiveness with which trains of intracellular action potentials actively back-propagate into the dendrites of hippocampal pyramidal cells (A–D, same as in the top panels).
