Autaptic Excitation Elicits Persistent Activity and a Plateau Potential in a Neuron of Known Behavioral Function

Abstract

Synaptic connections from a neuron onto itself (autapses) are not uncommon, but their contributions to information processing and behavior are not fully understood. Positive feedback mediated by autapses could in principle give rise to persistent activity, a property of some neurons in which a brief stimulus causes a long-lasting response. We have identified an autapse that underlies a plateau potential causing persistent activity in the B31/B32 neurons of Aplysia. The persistent activity is essential to the ability of these neurons to initiate and maintain components of feeding behavior. Persistent activity in B31/B32 arises from a voltage-dependent muscarinic autapse and from pharmacologically identical network-based positive feedback. Depolarization via the autapse begins later than network-driven excitation, and the effect of the autapse is therefore overshadowed by the earlier network-based depolarization. In B31/B32 neurons isolated in culture only the autapse is present, and the autapse functionally replaces the missing network-based feedback. Properties of B31/B32 provide insight into a possible general function of autapses. Autapses might function along with synapses from presynaptic neurons as components of feedback loops.

Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia

“…To examine whether changes in the mechanoafferent neurons could affect the initiation of feeding, we examined whether the mechanoafferent neurons affect B31/B32. These two neurons have a key role in deciding to initiate a consummatory feeding response (Hurwitz et al 2008;Saada et al 2009). In addition, the B31/B32 neurons innervate the I2 muscle (Hurwitz et al 1994(Hurwitz et al , 2000, whose activity causes radula protraction (Hurwitz et al 1996).…”

“…However, neurons that are electrically coupled to either the presynaptic or postsynaptic neuron may fire, since they are not depolarized by transmitter release. B31/B32 are electrically coupled to B63, which in turn excites B31/B32 via fast (Hurwitz et al 1997) and slow EPSPs (Saada et al 2009). In addition to being electrically coupled to B31/B32, B63 also has a lower firing threshold than does the B31/B32 axon Saada et al 2009).…”

“…B31/B32 are electrically coupled to B63, which in turn excites B31/B32 via fast (Hurwitz et al 1997) and slow EPSPs (Saada et al 2009). In addition to being electrically coupled to B31/B32, B63 also has a lower firing threshold than does the B31/B32 axon Saada et al 2009). Recordings from B31/ B32 after firing buccal ganglia mechanoafferents showed fast EPSPs from B63 (Fig.…”

“…3A1), in addition to direct EPSPs from the mechanoafferent cell. Since B63 elicits both fast and slow excitation of B31/B32 (Dembrow et al 2004;Saada et al 2009), firing of B63 in response to mechanoafferent firing raises the possibility that some of the slow EPSPs elicited by the mechanoafferents may have been via B63 activity. However, this possibility is unlikely, since the slow EPSPs from mechanoafferents to B31/B32 were usually seen in the absence of fast B63 EPSPs, which occur every time that B63 fires, and B63 firing was present only after strong depolarization of B31/B32 that resulted from a slow EPSP (see Fig.…”

“…3A1). In addition, the slow EPSPs that result from B63 firing are generally elicited at high B63 firing frequencies (Saada et al 2009), which were never seen.…”