Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

Abstract

Computational modeling assists in analyzing the specific functional role of the cellular effects of acetylcholine within cortical structures. In particular, acetylcholine may regulate the dynamics of encoding and retrieval of information by regulating the magnitude of synaptic transmission at excitatory recurrent connections. Many abstract models of associative memory function ignore the influence of changes in synaptic strength during the storage process and apply the effect of these changes only during a socalled recall-phase. Efforts to ensure stable activity with more realistic, continuous updating of the synaptic strength during the storage process have shown that the memory capacity of a realistic cortical network can be greatly enhanced if cholinergic modulation blocks transmission at synaptic connections of the association fibers during the learning process. We here present experimental data from an olfactory cortex brain slice preparation showing that previously potentiated fibers show significantly greater suppression (presynaptic inhibition) by the cholinergic agonist carbachol than unpotentiated fibers. We conclude that low suppression of non-potentiated fibers during the learning process ensures the formation of self-organized representations in the neural network while the higher suppression of previously potentiated fibers minimizes interference between overlapping patterns. We show in a computational model of olfactory cortex, that, together, these two phenomena reduce the overlap between patterns that are stored within the same neural network structure. These results further demonstrate the contribution of acetylcholine to mechanisms of cortical plasticity. The results are consistent with the extensive evidence supporting a role for acetylcholine in encoding of new memories and enhancement of response to salient sensory stimuli.

Scopolamine infused into perirhinal cortex improves object recognition memory by blocking the acquisition of interfering object information

“…Moreover, ACh has been implicated in synaptic plasticity processes within PRh (Massey et al 2001;Warburton et al 2003), and this function is probably related to the role of ACh in enhancing cortical information processing (Sarter and Bruno 1997;Rasmusson 2000). The present interpretation is consistent with the view that increased cortical ACh levels encourage encoding by enhancing afferent input and suppressing excitatory intrinsic circuitry (Hasselmo and Bower 1993;Linster et al 2003;Hasselmo and McGaughy 2004). IntraPRh infusions of scopolamine administered before the acquisition of new object information may disrupt such a process, reducing the selectivity of cortical responsiveness to incoming sensory information about the object being explored.…”

Focusing Effect of Acetylcholine on Neuroplasticity in the Human Motor Cortex

“…The diminution of the anodal tDCS-induced excitability enhancement might thus be because of an ACh-induced decrease of general excitation within global neuronal networks, probably modulated via the cholinergic presynaptic inhibition of excitatory feedback potentials or excitatory transmission at recurrent connections. Moreover, evidence reveals that the suppression of synaptic transmission is selective for recently modified synapses (Linster et al, 2003) but does not apply to silent synapses (Fernandez de Sevilla et al, 2002). Thus it is probable that synapses that are globally modified by tDCS in the present study are more susceptible to cholinergic suppression of synaptic transmission during plasticity induction.…”

Odor-specific habituation arises from interaction of afferent synaptic adaptation and intrinsic synaptic potentiation in olfactory cortex

“…However, the experience dependence suggests that there may be an additional process involved. In fact, theoretical views of piriform cortical function suggest that the cortex learns previous patterns of input via potentiation of intracortical association fiber synapses (Hasselmo et al 1990;Barkai et al 1994;Haberly 2001;Linster et al 2003). This autoassociative process essentially creates a template of previous network activity, against which new input patterns can be compared, allowing enhanced discrimination between similar patterns, as well as completion of degraded patterns (Barkai et al 1994;Barnes et al 2008).…”