Laminar Selectivity of the Cholinergic Suppression of Synaptic Transmission in Rat Hippocampal Region CA 1: Computational Modeling and Brain Slice Physiology

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Laminar Selectivity of the Cholinergic Suppression of Synaptic Transmission in Rat Hippocampal Region CA 1: Computational Modeling and Brain Slice Physiology The Journal of Neuroscience, June 1994, 14(6): 38983914 Laminar Selectivity of the Cholinergic Suppression of Synaptic Transmission in Rat Hippocampal Region CA 1: Computational Modeling and Brain Slice Physiology Michael E. Hasselmo and Eric Schnell Department of Psychology and Program in Neuroscience, Harvard University, Cambridge, Massachusetts 02138 ACh may set the dynamics of cortical function to those ap- ACh suppressesexcitatory synaptic transmissionin many regions propriate for learning new information. In models of the pu- of the cortex, including the piriform cortex (Williams and Con- tative associative memory function of piriform cortex, se- stanti, 1988; Hasselmo and Bower, 1992) the dentate gyrus lective suppression of intrinsic but not afferent fiber synaptic (Yamamoto and Kawai, 1967; Kahle and Cotman, 1989; Bur- transmission by ACh prevents recall of previous input from gard and Sarvey, 1990) region CA1 of the hippocampus interfering with the learning of new input (Hasselmo, 1993). (Hounsgaard, 1978; Valentino and Dingledine, 1981; Dutar and Selective cholinergic suppression may play a similar role in Nicoll, 1988; Blitzer et al., 1990; Sheridan and Sutor, 1990) the hippocampal formation, where Schaffer collateral syn- and neocortical structures (Brother et al., 1992). The memory apses in stratum radiatum (s. rad) may store associations impairment causedby muscarinic antagonistsor lesionsof cor- between activity in region CA3 and the entorhinal cortex tical cholinergic innervation (Beatty and Carbone, 1980; Walker input to region CA1 terminating in stratum lacunosum-mo- and Olton, 1984; Spenceret al., 1985; Kopelman, 1986; Hagan leculare (s. l-m). A computational model of region CA1 pre- and Morris, 1989) may be due to blockade of this cholinergic dicts that for effective associative memory function of the suppression. Computational modeling suggeststhat selective Schaffer collaterals, cholinergic suppression of synaptic cholinergic suppressionof synaptic transmission may be essen- transmission should be stronger in s. rad than in s. l-m. tial to associative memory function within cortical structures In the hippocampal slice preparation, we tested the effect (Hasselmoet al., 1992; Hasselmo, 1993, 1994; Hasselmoand of the cholinergic agonist carbachol (0.01-500 PM) on syn- Bower, 1993; Barkai and Hasselmo, 1994b). aptic transmission in s. rad and s. l-m. Stimulating and re- Associative memory function involves the learned capacity cording electrodes were simultaneously placed in both lay- for a specific pattern of activity in one population of cortical ers, allowing analysis of the effect of carbachol on synaptic neurons to elicit an associatedpattern of activity in another potentials in both layers during the same perfusion in each population of cortical neurons(Grossberg, 1970; Anderson, 1972, slice. Carbachol produced a significantly stronger suppres- 1983; Amit, 1988; Kohonen, 1988; Hasselmoet al., 1992; Has- sion of stimulus-evoked EPSPs in s. rad than in s. I-m at all selmo, 1993, 1994). Learning of theseassociations is commonly concentrations greater than 1 FM. At 100 PM, EPSP initial obtained by strengtheningexcitatory synapsesbetween neurons slopes were suppressed by 89.1 * 3.0% in s. rad, but only based on concurrent pre- and postsynaptic activity (e.g., the by 40.1 + 4.1% in s. l-m. The muscarinic antagonist atropine Hebb rule). However, to prevent recall of previously learned (1 PM) blocked cholinergic suppression in both layers. These associationsfrom altering the new association, the modifiable data support the hypothesis that synaptic modification of synapsesmust not be the predominant influence on postsynaptic the Schaffer collaterals may store associations between ac- activity during learning (Hasselmoet al., 1992; Hasselmo,1993). tivity in region CA3 and the afferent input to region CA1 from If modifiable synapsesare the predominant influence on post- the entorhinal cortex. In simulations, feedback regulation of synaptic activity during learning, then these synapsesundergo cholinergic modulation based on activity in region CA1 sets self-organization (Von der Malsburg, 1973; Grossberg, 1976; the appropriate dynamics of learning for novel associations, Linsker, 1988; Miller et al., 1989; Hasselmo, 1994). and recall for familiar associations. In the piriform (olfactory) cortex (seeFig. l), ACh selectively [Key words: ACb, hippocampus, associative memory, self- suppressessynaptic transmissionat excitatory intrinsic synapses organization, synaptic modification, presynaptic inhibition, between pyramidal cells, while having little effect on synaptic muscarinic, stratum radiatum, stratum lacunosum-molecu- transmission at afferent fibers arising from the olfactory bulb /are] (Hasseimoand Bower, 1992). In modelsofpiriform cortex (Has- selmo et al., 1992; Barkai and Hasselmo, 1994a,b; Hasselmo, 1993, 1994) suppressionof intrinsic fiber synaptic transmission Received Sept. 10, 1993; revised Dec. 13, 1993; accepted Dec. 31, 1993. during learning prevents the recall of previously stored associ- This work was supported by an Office of Naval Research Young Investigator ations from interfering with the learning of new associations. Award and the French Foundation for Alzheimer Research. We thank Edi Barkai for experimental assistance, John Holena for simulation piogramming, and Matt At the sametime, the weaker influence on afferent fiber synapses Wilson for the data collection and graphics software. allows them to undergo self-organization, and to set the pattern Correspondence should be addressed to Prof. Michael E. Hasselmo, Department of activity to be learned (Hasseimo, 1994). of Psychology, Room 950, Harvard University, 33 Kirkland Street, Cambridge, MA 02138. Theseresults may apply to cholinergic modulation of memory Copyright 0 1994 Society for Neuroscience 0270.6474/94/143898-17$05.00/O function in the hippocampusas well. As shown in Figure 1, the The Journal of Neuroscience, June 1994, 74(6) 3899 pyramidal cells of region CA1 receive excitatory synaptic input from different cortical regions in different layers. In the proximal layer, stratum radiatum (s. rad), these neurons receive excitatory synapses of the Schaffer collaterals, which arise from region CA3 (see Amaral and Witter, 1989, for review). In the distal layer, stratum lacunosum-moleculare (s. l-m), these neurons receive excitatory synapses of the perforant pathway arising from layer III ofthe entorhinal cortex (Lorente de No, 1938; Steward, 1976; Witter et al., 1988). A considerable amount of research has focused on the possible Hebbian nature of synaptic modification at the Schaffer collaterals (Kelso et al., 1986; Wigstrom et al., 1986; Gustafsson and Wigstrom, 1988). Some researchers have proposed that this Hebbian synaptic modification underlies het- eroassociative memory function at the Schaffer collaterals, al- lowing these synapses to store associations between the activity of region CA3 and the afferent input from entorhinal cortex (Levy, 1989; Eichenbaum and Buckingham, 1990; Levy et al., 1990; McNaughton, 199 1). This could allow the region to per- Piriform cortex form a comparison of the output of region CA3 with the current Afferent fibers afferent input from the entorhinal cortex (Levy, 1989; Eichen- baum and Buckingham, 1990; Levy et al., 1990). In contrast, OB other models have proposed that the Schaffer collaterals undergo competitive self-organization (Rolls, 199 1). The possible comparison function of region CA1 could allow activity in this area to reflect the novelty or familiarity of a NO pattern of afferent input, and thereby to regulate its own cho- linergic modulation for the appropriate dynamics of learning or recall. This comparison function requires that the Schaffer col- laterals have the capacity to perform effective heteroassociative memory function, rather than only to undergo self-organization. Intrinsic fibers The simulations presented here show that if the Schaffer col- laterals have heteroassociative memory function, this would Figure I. A, Schematic representation of hippocampal region CA1 require that ACh should suppress synaptic transmission more showing the laminar segregation of excitatory synapses. Perlorant path strongly in s. rad than in s. l-m. Previous studies have dem- fibers from the entorhinal cortex layer III (EC ZZZI terminate on the onstrated a strong cholinergic suppression of synaptic trans- distal dendrites of pyramidal cells instratum lacunosum-moleculare (3. mission at the Schaffer collateral-CA 1 synapse (Hounsgaard, I-m). Schaffer collateral axons arising from region CA3 pyramidal cells terminate on the proximal dendrites of pyramidal cells in stratum ra- 1978; Valentino and Dingledine, 198 1; Dutar and Nicoll, 1988; diatum (s. rud). In simulations, selective cholinergic suppression of Sheridan and Sutor, 1990) but no studies have analyzed the Schaffer collaterals allows them to store associations between activity effects of cholinergic modulation in s. l-m. In the experimental in region CA3 and the input from entorhinal cortex. Cholinergic sup- work presented here, we demonstrate that cholinergic suppres- pression of synaptic transmission at the Schaffer collaterals has been sion of synaptic transmission is indeed stronger in stratum ra- demonstrated (AC/z), but choline@ suppression of synaptic transmis- sion at the perforant path synapses in s. l-m has not been studied pre- diatum than in stratum lacunosum-moleculare, supporting the viously (No ACh.?). B, Schematic representation
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