STRUCTURAL SYNAPTIC CORRELATE OF LONG-TERM POTENTIATION - FORMATION OF AXOSPINOUS SYNAPSES WITH MULTIPLE, COMPLETELY PARTITIONED TRANSMISSION ZONES

Synapses were analyzed in the middle molecular layer (MML) and inner m olecular layer (IML) of the rat dentate gyrus following the induction of long-term potentiation (LTP) by high-frequency stimulation of the m edial perforant path carried out on each of 4 consecutive days. Potent iated animals were sacrificed 1 hour after the fourth high frequency s timulation. Stimulated but not potentiated and implanted but not stimu lated animals served as controls. Using the stereological disector tec hnique, unbiased estimates of the number of synapses per postsynaptic neuron were differentially obtained for various subtypes of axospinous junctions: For atypical (giant) nonperforated synapses with a continu ous postsynaptic density (PSD), and for perforated ones distinguished by (1) a fenestrated PSD and focal spine partition, (2) a horseshoe-sh aped PSD and sectional spine partition, (3) a segmented PSD and comple te spine partition(s), and (4) a fenestrated, (5) horseshoe-shaped, or (6) segmented PSD without a spine partition. The major finding of thi s study is that the induction of LTP in the rat dentate gyrus is follo wed by a significant and marked increase in the number of only those p erforated axospinous synapses that have multiple, completely partition ed transmission zones. No other synaptic subtype exhibits such a chang e as a result of LTP induction. Moreover, this structural alteration i s limited to the terminal synaptic field of activated axons (MML) and does not involve an immediately adjacent one (IML) that was not direct ly activated by potentiating stimulation. The observed highly selectiv e modification of synaptic connectivity involving only one particular synaptic subtype in the potentiated synaptic field may represent a str uctural substrate of the long-lasting enhancement of synaptic response s that characterizes LTP.