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Journal of Neuroscience, Vol 14, 3898-3914, Copyright © 1994 by Society for Neuroscience
Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology
ME Hasselmo and E Schnell
Department of Psychology, Harvard University, Cambridge, Massachusetts 02138.
ACh may set the dynamics of cortical function to those appropriate for
learning new information. In models of the putative associative memory
function of piriform cortex, selective suppression of intrinsic but not
afferent fiber synaptic transmission by ACh prevents recall of previous
input from interfering with the learning of new input (Hasselmo, 1993).
Selective cholinergic suppression may play a similar role in the
hippocampal formation, where Schaffer collateral synapses in stratum
radiatum (s. rad) may store associations between activity in region CA3 and
the entorhinal cortex input to region CA1 terminating in stratum
lacunosum-moleculare (s. l-m). A computational model of region CA1 predicts
that for effective associative memory function of the Schaffer collaterals,
cholinergic suppression of synaptic transmission should be stronger in s.
rad than in s. l-m. In the hippocampal slice preparation, we tested the
effect of the cholinergic agonist carbachol (0.01-500 microM) on synaptic
transmission in s. rad and s. l-m. Stimulating and recording electrodes
were simultaneously placed in both layers, allowing analysis of the effect
of carbachol on synaptic potentials in both layers during the same
perfusion in each slice. Carbachol produced a significantly stronger
suppression of stimulus- evoked EPSPs in s. rad than in s. l-m at all
concentrations greater than 1 microM. At 100 microM, EPSP initial slopes
were suppressed by 89.1 +/- 3.0% in s. rad, but only by 40.1 +/- 4.1% in s.
l-m. The muscarinic antagonist atropine (1 microM) blocked cholinergic
suppression in both layers. These data support the hypothesis that synaptic
modification of the Schaffer collaterals may store associations between
activity in region CA3 and the afferent input to region CA1 from the
entorhinal cortex. In simulations, feedback regulation of cholinergic
modulation based on activity in region CA1 sets the appropriate dynamics of
learning for novel associations, and recall for familiar associations.
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