Exploration-dependent modulation of evoked responses in fascia dentata: Fundamental observations and time course

Abstract

The hippocampal formation is thought to be involved in spatiallearning. A role as a more general, intermediate-term memory store has also been suggested. In this report, we address a moderately persistent change in propagation of excitation through hippocampal circuitry which resulted from exposure of animals to environments in which they were free to move and explore. Rats were prepared for chronic recording of perforant path-evoked dentate granule-cell population responses. A large increase in the synaptic component of this response developed over the first several minutes after the animals were transferred to a different but not necessarily novel environment, and decayed with a time constant of about 5 min. This apparent growth in synaptic strength was remarkably weIl correlated with the animal's recent history of exploratory behavior, and was not due simply to handling or to the electrical stimulation. The amplitude of the population-spike component also varied over time, but was not obviously correlated with changes in the synaptic component. These response changes were different in both apparent mechanism and time course from previously reported, longer lasting, environmentally induced changes in the population-spike component. They also differed from the behavioral state-dependent gating effect reported by Winson and Abzug (1977) to the extent that the present effects long outlasted the behaviors that produced them. Although further analysis is required, it is possible that this phenomenon may reflect one mode of information storage in the hippocampal formation.

Exploration-dependent modulation of evoked responses in fascia dentata: dissociation of motor, EEG, and sensory factors and evidence for a synaptic efficacy change

“…Third, as noted by Sharp et al (1989) during periods of intense locomotor activity such as transitions between environments or, as in the present experiments, treadmill walking, there was a substantial, but transient, decline in the field EPSP amplitude. The proportional reduction of EPSP amplitude during treadmill walking was independent of stimulus intensity over a broad range.…”

“…The EPSP reduction recovered immediately upon cessation of the treadmill activity. Sharp et al (1989) reported that this sort of attenuation did not occur in the absence of prior EPSP growth. In the present studies, we found that the attenuation was strictly proportional to the magnitude of the EPSP growth just prior to locomotor activity, rather than to the absolute amplitude of the EPSP itself.…”

“…Again, these changes outlasted the behavioral and EEG state changes. As shown by Sharp et al (1989), the EPSP change appears to be related to the time integral of the exploratory behavior, with a decay time constant of many minutes.…”

“…behavior in rats is accompanied by several slowly decaying alterations in the components of electrically evoked synaptic responses in the fascia dentata of the hippocampal formation (Sharp et al, 1985(Sharp et al, , 1986(Sharp et al, , 1989. These alterations include a robust increase in the magnitude of population EPSPs and a decrease in both the amplitude and the peak latency of evoked population spikes.…”

“…The synaptic response appeared to behave like a mathematical integrator of recent exploratory behavior, with a 5%15-min time constant. Most of the variance in the Sharp et al (1989) where EPSP reflects the synaptic response ~IOI.~IIN~IXY~ to its lowest baseline value, Ex is a measure of exploratory behavior. k, and kZ are positive constants.…”