In the Piriform Cortex, the Primary Impetus for Information Encoding through Synaptic Plasticity Is Provided by Descending Rather than Ascending Olfactory Inputs

When an animal is facing unfamiliar food, its odor, together with semiochemicals emanating from a conspecific, can constitute a safety message and authorize intake. The piriform cortex (PiC) codes olfactory information, and the inactivation of neurons in the nucleus accumbens (NAc) can acutely trigger consumption. However, the neural circuit and cellular substrate of transition of olfactory perception into value-based actions remain elusive. We detected enhanced activity after social transmission between two mice in neurons of the medial prefrontal cortex (mPFC) that target the NAc and receive projections from the PiC. Exposure to a conspecific potentiated the excitatory postsynaptic currents in NAc projectors, whereas blocking transmission from PiC to mPFC prevented social transmission. Thus, synaptic plasticity in the mPFC is a cellular substrate of social transmission of food safety.

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Regulation of hippocampal information encoding by metabotopic glutamate receptors

Neuroforum ◽

10.1515/nf-2018-a007 ◽

2018 ◽

Vol 24 (3) ◽

pp. A121-A126

Author(s):

Denise Manahan-Vaughan

Keyword(s):

Synaptic Plasticity ◽

Glutamate Receptors ◽

Ampa Receptors ◽

Receptor Activation ◽

Information Storage ◽

Long Term Memory ◽

Information Encoding ◽

Metabotropic Glutamate ◽

Long Term Storage

Abstract The hippocampus supports the acquisition of both spatial representations and long-term spatial memory. This is enabled by a triumvirate of physiological processes comprising information organisation and transfer by means of neuronal oscillations, creation of context-dependent spatial maps by means of place cells, and long-term storage of spatial experience by means of synaptic plasticity. All three processes are enabled by the glutamatergic system. Glutamate binding to ionotropic glutamate receptors enables both fast excitatory synaptic transmission (via AMPA receptors) and the initiation of long-term synaptic storage (via NMDA receptors). But glutamate also binds to metabotropic glutamate (mGlu) receptors. These receptors not only contribute to the stability of hippocampal encoding and the longevity of synaptic plasticity, they can also support synaptic information storage independent of NMDA receptor activation and are important for the acquisition and retention of long-term memory.

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Presynaptic mitochondria volume and abundance increase during development of a high-fidelity synapse

10.1101/689653 ◽

2019 ◽

Author(s):

Connon I. Thomas ◽

Christian Keine ◽

Satoko Okayama ◽

Rachel Satterfield ◽

Morgan Musgrove ◽

...

Keyword(s):

Synaptic Plasticity ◽

Adenoviral Vector ◽

Auditory Brainstem ◽

Auditory Information ◽

Developmental Profile ◽

Calyx Of Held ◽

Information Encoding ◽

Firing Rates ◽

Block Face ◽

High Firing

AbstractThe calyx of Held, a large glutamatergic presynaptic terminal in the auditory brainstem undergoes developmental changes to support the high action-potential firing rates required for auditory information encoding. In addition, calyx terminals are morphologically diverse which impacts vesicle release properties and synaptic plasticity. Mitochondria influence synaptic plasticity through calcium buffering and are crucial for providing the energy required for synaptic transmission. Therefore, it has been postulated that mitochondrial levels increase during development and contribute to the morphological-functional diversity in the mature calyx. However, the developmental profile of mitochondrial volumes and subsynaptic distribution at the calyx of Held remains unclear. To provide insight on this, we developed a helper-dependent adenoviral vector (HdAd) that expresses the genetically encoded peroxidase marker for mitochondria, mito-APEX2, at the mouse calyx of Held. We developed protocols to detect labeled mitochondria for use with serial block face scanning electron microscopy to carry out semi-automated segmentation of mitochondria, high-throughput whole terminal reconstruction and presynaptic ultrastructure in mice of either sex. Subsequently, we measured mitochondrial volumes and subsynaptic distributions at the immature postnatal day 7 (P7) and the mature (P21) calyx. We found an increase of mitochondria volumes in terminals and axons from P7 to P21 but did not observe differences between stalk and swelling subcompartments in the mature calyx. Based on these findings, we propose that mitochondrial volumes and synaptic localization developmentally increase to support high firing rates required in the initial stages of auditory information processing.Significance StatementElucidating the developmental processes of auditory brainstem presynaptic terminals is critical to understanding auditory information encoding. Additionally, morphological-functional diversity at these terminals is proposed to enhance coding capacity. Mitochondria provide energy for synaptic transmission and can buffer calcium, impacting synaptic plasticity; however, their developmental profile to ultimately support the energetic demands of synapses following the onset of hearing remains unknown. Therefore, we created a helper-dependent adenoviral vector with the mitochondria-targeting peroxidase mito-APEX2 and expressed it at the mouse calyx of Held. Volumetric reconstructions of serial block face electron microscopy data of immature and mature labeled calyces reveal that mitochondrial volumes are increased to support high firing rates upon maturity.

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Scaling principles of distributed circuits

10.1101/449447 ◽

2018 ◽

Author(s):

Shyam Srinivasan ◽

Charles F Stevens

Keyword(s):

Visual Acuity ◽

Piriform Cortex ◽

Quantitative Relationship ◽

Functional Abilities ◽

Invariant Property ◽

Information Encoding ◽

Scalable Systems ◽

Distributed Circuits ◽

Olfactory Ability ◽

Circuit Components

AbstractDistributed circuits like the olfactory cortex, hippocampus, and cerebellum contain sub-circuits whose inputs distribute their axons over the entire circuit creating a puzzle of how information is encoded. One method for approaching the puzzle is to view them as scalable systems. In scalable systems the quantitative relationship between circuit components is conserved across brain sizes, and by mapping circuit size to functional abilities - e.g. visual acuity in the visual circuit - scientists have explained information encoding. This approach has not been applied to anti-map circuits as their scalability is unknown. To address this gap in knowledge, we obtained quantitative descriptions of the olfactory bulb and piriform cortex in six mammals using stereology techniques and light microscopy. We found that the olfactory circuit is scalable as it satisfies three requirements of scalable systems. First, quantitative relationships between circuit components are conserved: the number piriform neurons n scales with bulb glomeruli g as n ∼ g3/2. Second, the olfactory circuit has an invariant property: the average number of synapses between a bulb glomerulus and piriform neuron is one. Third, the olfactory circuit is symmorphic, i.e. olfactory ability improves with circuit size. Other distributed circuits with similar properties might also be scalable.

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Disinhibitory circuitry gates associative synaptic plasticity in olfactory cortex

10.1101/2020.09.24.312686 ◽

2020 ◽

Author(s):

Martha Canto-Bustos ◽

F. Kathryn Friason ◽

Constanza Bassi ◽

Anne-Marie M. Oswald

Keyword(s):

Synaptic Plasticity ◽

Pyramidal Neurons ◽

Piriform Cortex ◽

Inhibitory Neuron ◽

Long Term Potentiation ◽

Inhibitory Interneurons ◽

Sensory Stimuli ◽

Term Potentiation ◽

Cortical Responses

AbstractInhibitory microcircuits play an essential role in regulating cortical responses to sensory stimuli. Interneurons that inhibit dendritic or somatic integration in pyramidal neurons act as gatekeepers for neural activity, synaptic plasticity and the formation of sensory representations. Conversely, interneurons that specifically inhibit other interneurons can open gates through disinhibition. In the rodent piriform cortex, relief of dendritic inhibition permits long-term potentiation (LTP) of the recurrent synapses between pyramidal neurons (PNs) thought to underlie ensemble odor representations. We used an optogenetic approach to identify the inhibitory interneurons and disinhibitory circuits that regulate LTP. We focused on three prominent inhibitory neuron classes-somatostatin (SST), parvalbumin (PV), and vasoactive intestinal polypeptide (VIP) interneurons. We find that VIP interneurons inhibit SST interneurons and promote LTP through subthreshold dendritic disinhibition. Alternatively, suppression of PV-interneuron inhibition promotes LTP but requires suprathreshold spike activity. Thus, we have identified two disinhibitory mechanisms to regulate synaptic plasticity during olfactory processing.

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LRP4 mediated synaptic plasticity in the piriform cortex

10.21203/rs.3.rs-539406/v1 ◽

2021 ◽

Author(s):

Min Yan ◽

Hongyang Jing ◽

Mingtao Xiong ◽

Dong Lin ◽

Peng Chen ◽

...

Keyword(s):

Synaptic Plasticity ◽

Transmembrane Domain ◽

Low Density Lipoprotein ◽

Critical Role ◽

Piriform Cortex ◽

Density Lipoprotein ◽

Spine Density ◽

Excitatory Postsynaptic Current ◽

Density Lipoprotein Receptor ◽

The Central Nervous System

Abstract Background Low-density lipoprotein receptor-related protein 4(LRP4) plays a critical role in the central nervous system (CNS), including hippocampal synaptic plasticity, maintenance of excitatory synaptic transmission, fear regulation, as well as long-term enhancement. Results In this study, we found that Lrp4 was highly expressed in the piriform cortex and located in the second layer of the piriform cortex. When the transmembrane domain (TMD) and the intracellular domain (ICD) were missing, the Lrp4ECD/ECD mice appeared to be smaller, and the brain’s weight decreased, compared with the control mice. Simultaneously, finding food was prolonged for Lrp4ECD/ECD mice in the buried food-seeking test. In the piriform cortex of Lrp4ECD/ECD mice, the spine density of layer Ⅱ increased, and the frequency of both miniature excitatory postsynaptic current (mEPSC) and spontaneous excitatory postsynaptic current (sEPSC) enhanced. Conclusions This study indicated that LRP4 mediated synaptic plasticity in the piriform cortex. Moreover, it also suggested that TMD and ICD of LRP4 are nonnegligible for the LRP4 function in the piriform cortex.

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Reconciling contrast invariance and non-linear computation in cortical circuits

10.1101/2021.04.23.441165 ◽

2021 ◽

Author(s):

L. Bernáez Timón ◽

P. Ekelmans ◽

S. Konrad ◽

A. Nold ◽

T. Tchumatchenko

Keyword(s):

Synaptic Plasticity ◽

Piriform Cortex ◽

Mean Field ◽

Dependent Manner ◽

Cortical Circuits ◽

Stimulus Contrast ◽

Spiking Network ◽

Network Simulations ◽

Contrast Invariance ◽

Balanced Networks

AbstractNetwork selectivity for orientation is invariant to changes in the stimulus contrast in the primary visual cortex. Similarly, the selectivity for odor identity is invariant to changes in odorant concentration in the piriform cortex. Interestingly, invariant network selectivity appears robust to local changes in synaptic strength induced by synaptic plasticity, even though: i) synaptic plasticity can potentiate or depress connections between neurons in a feature-dependent manner, and ii) in networks with balanced excitation and inhibition, synaptic plasticity is a determinant for the network non-linearity. In this study, we investigate whether network contrast invariance is consistent with a variety of synaptic states and connectivities in balanced networks. By using mean-field models and spiking network simulations, we show how the synaptic state controls the non-linearity in the network response to contrast and how it can lead to the emergence of contrast-invariant or contrast-dependent selectivity. Different forms of synaptic plasticity sharpen or broaden the network selectivity, while others do not affect it. Our results explain how the physiology of individual synapses is linked to contrast-invariant selectivity at the network level.

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Orchestration of Hippocampal Information Encoding by the Piriform Cortex

Cerebral Cortex ◽

10.1093/cercor/bhz077 ◽

2019 ◽

Vol 30 (1) ◽

pp. 135-147 ◽

Cited By ~ 2

Author(s):

Christina Strauch ◽

Denise Manahan-Vaughan

Keyword(s):

Information Processing ◽

Piriform Cortex ◽

Long Term Potentiation ◽

Early Gene ◽

Perforant Path ◽

Dependent Manner ◽

Information Encoding ◽

Term Potentiation ◽

Processing And Storage ◽

Stimulation Of

Abstract The hippocampus utilizes olfactospatial information to encode sensory experience by means of synaptic plasticity. Odor exposure is also a potent impetus for hippocampus-dependent memory retrieval. Here, we explored to what extent the piriform cortex directly impacts upon hippocampal information processing and storage. In behaving rats, test-pulse stimulation of the anterior piriform cortex (aPC) evoked field potentials in the dentate gyrus (DG). Patterned stimulation of the aPC triggered both long-term potentiation (LTP > 24 h) and short-term depression (STD), in a frequency-dependent manner. Dual stimulation of the aPC and perforant path demonstrated subordination of the aPC response, which was nonetheless completely distinct in profile to perforant path-induced DG plasticity. Correspondingly, patterned aPC stimulation resulted in somatic immediate early gene expression in the DG that did not overlap with responses elicited by perforant path stimulation. Our results support that the piriform cortex engages in specific control of hippocampal information processing and encoding. This process may underlie the unique role of olfactory cues in information encoding and retrieval of hippocampus-dependent associative memories.

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Age-Dependent Contributions of NMDA Receptors and L-Type Calcium Channels to Long-Term Depression in the Piriform Cortex

International Journal of Molecular Sciences ◽

10.3390/ijms222413551 ◽

2021 ◽

Vol 22 (24) ◽

pp. 13551

Author(s):

Vishaal Rajani ◽

Aida Maziar ◽

Kwun Nok Mimi Man ◽

Johannes W. Hell ◽

Qi Yuan

Keyword(s):

Synaptic Plasticity ◽

Calcium Channels ◽

Piriform Cortex ◽

Confocal Imaging ◽

Receptor Expression ◽

Sprague Dawley ◽

Long Term Depression ◽

Age Dependent ◽

Fluorescent Immunohistochemistry

In the hippocampus, the contributions of N-methyl-D-aspartate receptors (NMDARs) and L-type calcium channels (LTCCs) to neuronal transmission and synaptic plasticity change with aging, underlying calcium dysregulation and cognitive dysfunction. However, the relative contributions of NMDARs and LTCCs in other learning encoding structures during aging are not known. The piriform cortex (PC) plays a significant role in odor associative memories, and like the hippocampus, exhibits forms of long-term synaptic plasticity. Here, we investigated the expression and contribution of NMDARs and LTCCs in long-term depression (LTD) of the PC associational fiber pathway in three cohorts of Sprague Dawley rats: neonatal (1–2 weeks), young adult (2–3 months) and aged (20–25 months). Using a combination of slice electrophysiology, Western blotting, fluorescent immunohistochemistry and confocal imaging, we observed a shift from an NMDAR to LTCC mediation of LTD in aged rats, despite no difference in the amount of LTD expression. These changes in plasticity are related to age-dependent differential receptor expression in the PC. LTCC Cav1.2 expression relative to postsynaptic density protein 95 is increased in the associational pathway of the aged PC layer Ib. Enhanced LTCC contribution in synaptic depression in the PC may contribute to altered olfactory function and learning with aging.

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