Inhibitory neurons in the anterior piriform cortex of the mouse: Classification using molecular markers

Suzuki, Norimitsu; Bekkers, John M.

doi:10.1002/cne.22295

Cited by 101 publications

(142 citation statements)

References 57 publications

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“…S3) (27). We confirmed that interneurons comprise a small fraction (approximately 4%) of layer 2 neurons in the PC, consistent with previous reports (28). Thus, most of the neurons imaged in layer 2 are glutamatergic (SL and SP cells).…”

Section: Resultssupporting

confidence: 92%

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Tantirigama

Huang

Bekkers

2017

Proc. Natl. Acad. Sci. U.S.A.

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Neurons in the neocortex exhibit spontaneous spiking activity in the absence of external stimuli, but the origin and functions of this activity remain uncertain. Here, we show that spontaneous spiking is also prominent in a sensory paleocortex, the primary olfactory (piriform) cortex of mice. In the absence of applied odors, piriform neurons exhibit spontaneous firing at mean rates that vary systematically among neuronal classes. This activity requires the participation of NMDA receptors and is entirely driven by bottom-up spontaneous input from the olfactory bulb. Odor stimulation produces two types of spatially dispersed, odor-distinctive patterns of responses in piriform cortex layer 2 principal cells: Approximately 15% of cells are excited by odor, and another approximately 15% have their spontaneous activity suppressed. Our results show that, by allowing odor-evoked suppression as well as excitation, the responsiveness of piriform neurons is at least twofold less sparse than currently believed. Hence, by enabling bidirectional changes in spiking around an elevated baseline, spontaneous activity in the piriform cortex extends the dynamic range of odor representation and enriches the coding space for the representation of complex olfactory stimuli.T he brain remains intensely active even under conditions when overt external stimuli are absent (1). At first glance this behavior can seem puzzling. Pyramidal neurons in primary sensory neocortex, for example, typically fire spontaneously at approximately 1 Hz when the relevant stimuli are not present (2), raising the possibility that this background activity is noise that must be mitigated by signal averaging (3). On the other hand, spontaneous cortical activity is often structured (4) and can reflect the global state of the animal (5), suggesting that it is not simply an impediment but may serve a useful computational role. Indeed, such activity may be important for gating sensory inputs (4, 6), establishing and maintaining sensory maps (7-9), and extending the dynamic range of sensory-evoked responses (10, 11). The significance of spontaneous activity is also supported by theoretical studies showing that it emerges naturally from balanced neural networks with desirable information-processing characteristics (9, 12).Given that spontaneous spiking is likely to be a key element of cortical function, it is important to study its prevalence and properties in different cortical areas. The piriform cortex (PC) is a sensory paleocortex in mammals that is critical for recognizing and remembering odors (13-17). The PC offers a number of advantages for the study of neural information processing, including a simple trilaminar architecture and well-defined afferent input from the olfactory bulb (OB) (16, 17). As a phylogenetically "old" structure, the PC is also likely to express canonical cortical circuits that have been conserved across evolution (18). Spontaneous spiking has been reported in the PC of rodents breathing odor-free air (19-23), but these studies used unit r...

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Section: Resultssupporting

confidence: 92%

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Tantirigama

Huang

Bekkers

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Nonetheless, the increase in suppressive responses may suggest an important role for inhibitory interneurons in this plasticity. There are a variety of different classes of GABAergic interneurons in the aPCX each of which contribute differently to circuit function (Suzuki and Bekkers 2010). In naïve animals, inhibitory interneurons in piriform cortex are much more broadly odor responsive than pyramidal cells (Poo and Isaacson 2009).…”

Section: Discussionmentioning

confidence: 99%

Generalized vs. stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats

Chen

Barnes

Wilson

2011

Journal of Neurophysiology

100

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Chen CF, Barnes DC, Wilson DA. Generalized vs. stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats. J Neurophysiol 106: 3136 -3144, 2011. First published September 14, 2011 doi:10.1152/jn.00721.2011.-Experience shapes both central olfactory system function and odor perception. In piriform cortex, odor experience appears critical for synthetic processing of odor mixtures, which contributes to perceptual learning and perceptual acuity, as well as contributing to memory for events and/or rewards associated with odors. Here, we examined the effect of odor fear conditioning on piriform cortical single-unit responses to the learned aversive odor, as well as its effects on similar (overlapping mixtures) in freely moving rats. We found that odor-evoked fear responses were training paradigm dependent. Simple association of a condition stimulus positive (CSϩ) odor with foot shock (unconditioned stimulus) led to generalized fear (cue-evoked freezing) to similar odors. However, after differential conditioning, which included trials where a CSϪ odor (a mixture overlapping with the CSϩ) was not paired with shock, freezing responses were CSϩ odor specific and less generalized. Pseudoconditioning led to no odor-evoked freezing. These differential levels of stimulus control over freezing were associated with different training-induced changes in single-unit odor responses in anterior piriform cortex (aPCX). Both simple and differential conditioning induced a significant decrease in aPCX single-unit spontaneous activity compared with pretraining levels while pseudoconditioning did not. Simple conditioning enhanced mean receptive field size (breadth of tuning) of the aPCX units, while differential conditioning reduced mean receptive field size. These results suggest that generalized fear is associated with an impairment of olfactory cortical discrimination. Furthermore, changes in sensory processing are dependent on the nature of training and can predict the stimuluscontrolled behavioral outcome of the training. piriform cortex; fear conditioning; learning-induced plasticity THE OLFACTORY SYSTEM INVOLVES a memory-based odor processing function that allows its acuity to be constantly shaped by experience (Wilson and Stevenson 2006). This function enables animals to not only identify myriad novel odors and odor combinations in the environment but also to associate odors with their ecological significance, which is critical for adaptive behavior. Experience-dependent perceptual changes (perceptual learning) and their underlying neural plasticity have been reported across phylogeny from the first to third order neurons in the olfactory system (Davis 2004).

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“…In the piriform cortex, most excitatory neurons are clustered in layer II, while GABAergic interneurons are sparsely spread across all layers, as shown in Fig. 3 (Kapur et al, 1997;Ekstrand et al, 2001;Suzuki and Bekkers, 2007, 2010a, 2010b. Among excitatory neurons, semilunar cells are particularly concentrated in the outer part of layer II, where most DCX/PSA-NCAM IN can be found in the piriform cortex of mice and rats (Gómez-Climent et al, 2008;Rubio et al, 2015).…”

Section: The Number Of Dcx/psa-ncam In Declines Drastically With Agementioning

confidence: 92%

Distribution and fate of DCX/PSA-NCAM expressing cells in the adult mammalian cortex: A local reservoir for adult cortical neuroplasticity?

et al. 2016

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The expression of early developmental markers such as doublecortin (DCX) and the polysialylated-neural cell adhesion molecule (PSA-NCAM) has been used to identify immature neurons within canonical neurogenic niches. Additionally, DCX/PSA-NCAM + immature neurons reside in cortical layer II of the paleocortex and in the paleo-and entorhinal cortex of mice and rats, respectively. These cells are also found in the neocortex of guinea pigs, rabbits, some afrotherian mammals, cats, dogs, non-human primates, and humans. The population of cortical DCX/PSA-NCAM + immature neurons is generated prenatally as conclusively demonstrated in mice, rats, and guinea pigs. Thus, the majority of these cells do not appear to be the product of adult proliferative events. The immature neurons in cortical layer II are most abundant in the cortices of young individuals, while very few DCX/PSA-NCAM + cortical neurons can be detected in aged mammals. Maturation of DCX/PSA-NCAM + cells into glutamatergic and GABAergic neurons has been proposed as an explanation for the age-dependent reduction in their population over time. In this review, we compile the recent information regarding the age-related decrease in the number of cortical DCX/PSA-NCAM + neurons. We compare the distribution and fates of DCX/PSA-NCAM + neurons among mammalian species and speculate their impact on cognitive function. To respond to the diversity of adult neurogenesis research produced over the last number of decades, we close this review by discussing the use and precision of the term "adult non-canonical neurogenesis."

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Inhibitory neurons in the anterior piriform cortex of the mouse: Classification using molecular markers

Cited by 101 publications

References 57 publications

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Generalized vs. stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats

Distribution and fate of DCX/PSA-NCAM expressing cells in the adult mammalian cortex: A local reservoir for adult cortical neuroplasticity?

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