Dopamine induces LTP differentially in apical and basal dendrites through BDNF and voltage-dependent calcium channels

Abstract

The dopaminergic modulation of long-term potentiation (LTP) has been studied well, but the mechanism by which dopamine induces LTP (DA-LTP) in CA1 pyramidal neurons is unknown. Here, we report that DA-LTP in basal dendrites is dependent while in apical dendrites it is independent of activation of L-type voltage-gated calcium channels (VDCC). Activation via NMDAR is critical for the induction of DA-LTP in both apical and basal dendrites, but only BDNF is required for the induction and maintenance of DA-LTP in apical dendrites. We report that dopaminergic modulation of LTP is lamina-specific at the Schaffer collateral/commissural synapses in the CA1 region.In the hippocampus, afferent inputs to the hippocampus CA1 occur via two major pathways, the temporoammonic and the Schaffer collateral/commissural fibers. Among these, the Schaffer collateral/commissural fibers from the CA3 region synapse on both the apical dendrites in the stratum radiatum (str. radiatum) and the basal dendrites in the stratum oriens (str. oriens).Studies of long-term potentiation (LTP) in the hippocampal slices both in vitro and in vivo have shown that the threshold for inducing LTP is lower in basal dendrites in comparison to apical dendrites (Kaibara and Leung 1993;Leung and Shen 1995;Sajikumar et al. 2007;Stramiello and Wagner 2010;Sajikumar and Korte 2011a). The CA1 region receives a variety of neuromodulatory inputs including the dopaminergic, cholinergic, and noradrenergic pathways (Otmakhova and Lisman 2000;Leung et al. 2003), and the distributions of these neuromodulatory inputs are not uniform. For example, the hippocampus receives dispersed cholinergic innervations with the highest density of cholinergic axons in the str. oriens and principal cell layer (Arai et al. 1994;Gasbarri et al. 1994b;Aznavour et al. 2002), and anatomical studies suggest that, not only the str. radiatum but also the str. oriens, is innervated by dopaminergic projections from the meso-limbo-cortical system (Verney et al. 1985; Gasbarri et al. 1994a,b) The neuromodulatory influences in the str. radiatum and str. oriens regions are also different. One example of a spatially restricted effect of a neuromodulatory neurotransmitter is the action of acetylcholine on the muscarinic acetylcholine receptors. Cholinergic activation by carbachol produces a significantly stronger suppression of synaptic transmission at the CA3-CA1 synapses of the proximal apical dendrites, while being less effective at synapses of the apical tuft (Hasselmo and Schnell 1994). This cholinergic suppression has been shown to enhance associative memory functions (De Rosa and Hasselmo 2000). In neocortical pyramidal neurons, pairing of excitatory post-synaptic potentials (EPSPs) and action potentials (Gordon et al. 2006) leads to the potentiation of synapses at the proximal basal dendrites but not the distal basal dendrites. In the distal basal dendrites, synaptic potentiation occurs only when synaptic activation (which is strong enough to evoke an NMDA spike) is paired with BDNF applicatio...

Fear Memory

“…Dopaminergic and noradrenergic afferents modulate hippocampal LTP and LTD (155,221,456). Cholinergic substances also do, through nicotinic receptors (673).…”

Long-term depression is differentially expressed in distinct lamina of hippocampal CA1 dendrites

“…The mechanisms of induction and maintenance of LTP are different in apical and basal dendrites of CA1 pyramidal neurons (Arai et al, 1994; Kramár and Lynch, 2003; Sajikumar et al, 2007; Navakkode et al, 2012; Fan, 2013). But LTD expression in apical vs. basal dendrites is not well studied.…”

“…For example, the threshold for LTP is lower in proximal apical dendrites than in distal apical dendrites (Sajikumar and Korte, 2011), while the threshold for LTP in basal dendrites is reportedly similar to that in distal apical dendrites (Sajikumar et al, 2007), although different stimulation protocols were used in each region in the latter report. In addition, in a comparison of dopamine-induced LTP in basal and distal apical dendrites, expression of LTP in basal dendrites required L-type voltage-gated calcium channels, and expression of LTP in distal apical dendrites required BDNF (Navakkode et al, 2012). …”

Chronic constant light-induced hippocampal late-phase long-term potentiation impairment in vitro is attenuated by antagonist of D1/D5 receptors

“…Spatial memory and L-LTP were impaired while E-LTP was normal in D1 receptor knockout mice (Matthies et al, 1997). In addition, enhancement of D1/D5 receptors-mediated signaling cascade by drugs occluded tetanization-elicited L-LTP in hippocampal CA1 in vitro (Huang and Kandel, 1995;Navakkode et al, 2012). Besides, D1/D5 receptors agonists enhanced hippocampus-dependent memory and converted E-LTP into L-LTP at hippocampal SC-CA1 pathway (Bernabeu et al, 1997;Lemon and Manahan-Vaughan, 2006;Rossato et al, 2009).…”