An Early Critical Period for Long-Term Plasticity and Structural Modification of Sensory Synapses in Olfactory Cortex

Abstract

Critical periods for plasticity of thalamic sensory inputs play an important role in developing neocortical circuits. During an early postnatal time window, pyramidal cells of visual, auditory, and somatosensory cortex undergo structural refinement and possess an enhanced ability for activity-dependent synaptic plasticity. In olfactory cortex, however, pyramidal cells receive direct sensory input from the olfactory bulb, and it is unclear whether the development of olfactory sensory circuits is governed by a critical period. Here, we show that NMDA receptor-dependent long-term potentiation and dendritic spine maturation occur only during a brief postnatal time window at sensory synapses of olfactory cortex pyramidal cells. In contrast, associational synapses onto the same cells retain the capacity for plasticity into adulthood.

Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

“…After a brief postnatal critical period, NMDAR-dependent LTP in layer 2/3 cells of the anterior piriform cortex is more pronounced in the associative layer 1b than in the sensory layer 1a synapses (Jung et al, 1990a,b;Kanter and Haberly, 1990;Franks and Isaacson, 2005;Poo and Isaacson, 2007). Looking for a mechanistic explanation for this phenomenon, we observed striking differences between layer 1a and layer 1b in the spine Ca 2ϩ transients underlying LTP induction.…”

“…6 B). Selective stimulation of layer 1a by pharmacological block of layer 1b synapses with baclofen has been demonstrated previously (Franks and Isaacson, 2005;Poo and Isaacson, 2007); however, it is important to note that GABA B receptors activate dendritic K ϩ conductances and inhibit voltage-gated calcium channels (VGCCs) in the postsynaptic cell (Pérez-Garci et al, 2006). The pharmacological isolation approach thus activates mechanisms that diminish layer 1a Ca 2ϩ responses evoked by bAPs and is therefore unsuited for our study.…”

“…A key functional difference between the two synaptic inputs is their plasticity. NMDA receptor (NMDAR)-dependent long-term potentiation (LTP) of synaptic contacts is much more pronounced in the proximal associative layer 1b than in the distal sensory layer 1a (Jung et al, 1990a,b;Kanter and Haberly, 1990;Franks and Isaacson, 2005;Poo and Isaacson, 2007). So far, mechanisms determining the weakness of layer 1a LTP have only been found on the level of LTP expression (Franks and Isaacson, 2005).…”

Two Layers of Synaptic Processing by Principal Neurons in Piriform Cortex

“…However, stimulation of aff inputs can often lead to polysynaptic excitation of assn fibers, complicating the interpretation. One way to overcome this problem is to bath-apply the GABA B agonist, baclofen, which has been reported to selectively block assn inputs onto layer II SP cells (Tang and Hasselmo, 1994), thereby allowing pharmacological isolation of aff inputs onto pyramidal cells Isaacson, 2005, 2006;Poo and Isaacson, 2007). Hence, we began by checking whether baclofen is also useful for isolating aff inputs onto SL cells.…”

“…This approach has so far identified, for example, classes of glutamate-releasing principal neurons (Franks and Isaacson, 2006;Suzuki and Bekkers, 2006), their dendritic properties (Bathellier et al, 2009), circuits and synaptic plasticity (Franks and Isaacson, 2005;Poo and Isaacson, 2007;Johenning et al, 2009), and classes of GABA-releasing interneurons and their circuits (Young and Sun, 2009;Stokes and Isaacson, 2010;Suzuki and Bekkers, 2010a,b). We have previously reported that the main input layer of the PC, layer II, contains two functionally distinctive kinds of principal neurons, semilunar (SL) and superficial pyramidal (SP) cells (Suzuki and Bekkers, 2006).…”