The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization

Dendritic spines are tiny, specialized protoplasmic protuberances that cover the surface of many neurons. First described by Ramon y Cajal ( 1991) in light microscopic studies of Golgistained tissue, they are among the most striking subcellular features of many neurons. Spines serve as the major target for excitatory synaptic input onto principal neurons in the hippocampus, the neocortex, and other brain regions. Their intimate association with synaptic traffic suggests some critical role in synaptic transmission and plasticity. We here review experimental data and theoretical models with respect to the putative role of dendritic spines in the induction and retention of synaptic plasticity. The ubiquity of spines demands explanation, yet their small size- near the limit of resolution of light microscopy- impedes an experimental frontal assault. Until recently, most theoretical studies focused on the role of the spine neck geometry in regulating the amplitude of the EPSP received at the soma. However, recent experimental evidence suggests that the spine shape may not be able to modulate the "synaptic weight" effectively. Consequently, both theoretical models and calcium-imaging experiments are now focusing on the role of spines in amplifying and isolating calcium signals, particularly those involved in the induction of a calcium-dependent form of long-term synaptic plasticity. Until recently, physiological hypotheses about the function of the dendritic spines could only be explored indirectly, through analytical and computational studies based on morphological data. Recent technical advances in the direct visualization of calcium dynamics in dendritic structures are now permitting direct tests of some of these theoretical inferences. Three principal hypotheses have been advanced to explain the function of spines: ( 1) spines connect axons with dendrites, (2) spines shape the membrane potential in response to synaptic input, and (3) spines determine the dynamics of intracellular second messengers such as calcium. In this article we review the current status of each of these proposals with particular emphasis on the putative role of spines in the induction of a cellular model of synaptic plasticity in cortical structures, longterm potentiation (L TP). It may well be possible that dendritic spines serve some crucial role in normal synaptic transmission (D. Purves, personal communication). However, in this article we focus on their possible role in synaptic plasticity. Furthermore, we will not discuss the electrical behavior of that minority of spines in neocortex that carry both an excitatory and an inhibitory synapse (see Koch and Poggio, l983a; Qian and Sejnowski, 1989, 1990; Dehay et al., 1991 ), nor will we consider the role of dendrodendritic synapses, such as those found on the spines of olfactory granule cells (Rail and Shepherd, 1968; Shepherd and Greer, 1989)