Information processing and storage in the nervous system is generally thought to be
determined by the spatial and temporal firing patterns between interconnected populations
of neurons. Studies of connectivity and neuronal activity within the primate cerebral
cortex have demonstrated that layer V pyramidal neurons of the prefrontal cortex
transition between states of high and low activity, and these transitions correlate with
the on- and offset of the delay period in a working memory task. We have recently
demonstrated that internal Ca2+ release in these neurons can elicit a
hyperpolarization that suppresses firing and that spike trains that simulate neuronal
activity observed during working memory are capable of priming internal
Ca2+ release. These observations suggest that tonic firing or PFC layer V
pyramidal neurons primes the ER for Ca2+ release; subsequent internal
Ca2+ release activates an outward, hyperpolarizing current that suppresses
action potential generation, terminating the spike train. I believe that
Ca2+ released from the ER represents a powerful intracellular signal
important not only for general cellular function, but also for modulation of neuronal
activity, and that past neuronal activity is an important factor in determining whether
intracellular release of Ca2+ will occur. I hypothesize that neuronal
endoplasmic reticulum (ER), through its role as both a source and sink of
Ca2+, can both sense and modulate neuronal activity. This raises the
intriguing possibility that ER may act as a sensor of neuronal activity, which in turn
might alter neuronal function through the release of Ca2+. Consistent with
this possibility, anecdotal reports suggest that it is possible to "prime" the ER to
release Ca2+ by depolarizing neurons. Depolarization triggers
Ca2+ influx through voltage-gated Ca2+ channels (VGCCs), and
the uptake of this Ca2+ into the ER may increase the likelihood of
subsequent release from the ER. We have evidence suggesting that the relationship between
neuronal activity, loading of the ER with Ca2+, andInsP3-sensitive internal
Ca2+ release can regulate patterns of firing in the prefrontal cortex
(PFC)that are critical for performing working memory tasks. As a first step in determining
whether ER can act as a sensor of neuronal activity I propose to initiate a series of
experiments investigating the possibility that physiologically realistic patterns of
neuronal activity can lead to facilitated Ca2+ releasefrom the ER
and that this release can modulate subsequent neuronal activity. We will test these
hypotheses by using a combination of whole-cell patch-clamp recording and
Ca2+fluorescence imaging on layer V pyramidal neurons from acute rat PFC
slices. More specifically, our first aim will be to characterize the interactions between
neuronal activity andInsP3-mediated internal Ca2+ release. In our second
aim, we will examine more directly whether Ca2+ influx during neuronal
activity leads to priming by loading the ER. Our third aim will beto examine the
functional relationship between priming of internal Ca2+ release from the
ER and changes in neuronal activity under physiologically relevant conditions.